Chapter 3
Life History and Development
Oldrich Nedv eˇ d1 and Alois Hon eˇ k2 1 Faculty of Science, University of South Bohemia and Institute of Entomology, Academy of Sciences, CZ 37005 C ˇ esk é Bud eˇjovice, Czech Republic 2 Department of Entomology, Crop Research Institute, CZ 16106 Prague 6, Czech Republic
Ecology and Behaviour of the Ladybird Beetles (Coccinellidae), First Edition. Edited by I. Hodek, H.F. van Emden, A. Honeˇk. © 2012 Blackwell Publishing Ltd. Published 2012 by Blackwell Publishing Ltd. 54 3.1 INTRODUCTION from spermatheca (receptaculum seminis) can enter during oviposition, and for oxygen diffusion. A. bipunc- Coccinellids are holometabolous , i.e. they have a tata possesses 40 – 50 pores in two rings, Platynaspis ‘ complete metamorphosis ’ , and pass through the fol- luteorubra have clusters of pores at both ends of the lowing stages: egg, larva, pupa and adult. Egg stage egg. Chilocorini have trumpet shaped structures lasts 15 – 20% of the total preimaginal developmental besides the tube like micropyles (Ricci & Stella 1988 ). time, larva 55– 65% and pupa 20– 25% (Hone ˇ k & The egg of Scymnus sinuanodulus has a rosette of 4– 11 Kocourek 1990 , Dixon 2000 ). cup- shaped and 13 – 20 semicircular structures that are like micropyles (Lu et al. 2002 ). The surface of the coccinellid egg (chorion , egg 3.2 EGG shell) is usually smooth, except for the eggs of Epil- achninae which bear a polygonal sculpture (Klaus- 3.2.1 Egg morphology nitzer 1969b ; Fig. 3.1 c), and Rhyzobius with a granular surface (Ricci & Stella 1988 ). The smooth surface Coccinellid eggs are usually elongate, oval or elliptic. may be soaked with an oily excretion provided by They vary in colour from almost transparent (Scymnus accessory glands of the mother. The excretion is col- louisianae ; Brown et al. 2003 ), light grey (Stethorus ), ourless, or rarely red (as in Calvia quatuordecimguttata ; yellowish (Halyzia ) through bright yellow (most Klausnitzer & Klausnitzer 1986 ) and contains defen- species) to dark orange (Chilocorini), sometimes green- sive or signalling alkanes (Hemptinne et al. 2000 ; ish (Klausnitzer 1969b ). They are laid either upright, Chapter 9 .). attached (glued) to the substrate by the lower end (Coc- The yolk of the egg contains many nutrients . cinellinae) or lying on their side (Scymninae, Coccid- During embryonic development of the A. bipunctata ulinae, Chilocorinae). The ‘ upper ’ or anterior pole egg mass, lipid and glycogen contents decline strongly, bears a ring of micropyles (Fig. 3.1 ) – pores in the while egg protein decline more slowly. Free carbohy- chorion (the egg shell) through which spermatozoa drates decline early in egg development and increase
(a) (b)
(c) (d)
Figure 3.1 SEM photographs of ladybird eggs. (a, b) Harmonia axyridis, (c, d) Cynegetis impunctata. (a, c) upper parts of eggs with ring of micropyle openings; (b) ring of micropyles; (d) detail of a micropyle opening. 56 O. Nedveˇ d and A. Honeˇk before hatching (Sloggett & Lorenz 2008 ). Energy per microlitres may be calculated as: V = L W 2π/6, where L unit egg mass is lowest in the generalist A. bipunctata , is length and W is the width of the egg (Takakura which also has relatively large eggs, and is highest in 2004 ). the specialized Anisosticta novemdecimpunctata , which The weight of the eggs of large species C. septem- has small eggs. punctata (15.4 mg adult dry mass) and small species A few days or hours before hatching the eggs become P. quatuordecimpunctata (3.7 mg adult dry mass) dif- greyish, because the larvae are visible through the fered little (0.20 versus 0.18 mg) (Hon eˇ k et al. 2008 ). chorion. The fi rst instar larvae of Coccinellinae and C. septempunctata produces a larger number of indi- Epilachninae may possess special structures on head vidually smaller eggs than C. transversoguttata (Kajita and prothorax called egg teeth which probably help et al. 2009 ) which has the same body size. Similarly, the larva in hatching. Hatched larvae rest some time Har. axyridis produces larger egg clusters with smaller on the empty egg shells, and may eat them. eggs (0.28 mm 3 ) than Har. yedoensis (0.36 mm 3 ) Ladybird eggs are defended chemically against pre- (Osawa & Ohashi 2008 ). Species of similar adult size dation, including that which is intra- guild, and they laying smaller eggs may incur higher costs per unit are suitable to varying degrees as food for other lady- mass than species laying larger eggs. More specialized birds (Rieder et al. 2008 ; Chapter 7 ). species reproducing at lower aphid densities may provide neonate larvae with more nutrients to facili- tate the fi nding of an aphid colony (Sloggett & Lorenz 3.2.2 Egg size 2008 ). The fi tness of young larvae is positively related to Insect species have a genetically fi xed maximum egg size. Starving fi rst instar larvae survived substan- number of ovarioles related to egg cluster size (see tially longer (using only each individual’ s yolk below) and/or a fi xed maximum size of each single reserves ) in large Coelophora bissellata (with egg egg – traits expressed with ample food and other volume 1.53 mm 3) than did three other Malayan favourable environmental conditions. With a limited species with egg volumes of 0.81 – 1.20 mm 3 (Ng food supply, the size of eggs may be reduced and their 1988 ). However, small eggs have a higher rate of number maintained, or decreased and their size embryonic development , which decreases the risk maintained. Coccinellids adopt the second strategy of egg predation (Majerus 1994 ). Developmental time (Stewart et a1. 1991a, b; Dixon & Guo 1993 ; see was 3.0 days in Har. yedoensis possessing larger eggs also 5.2.3 ). This is similar to birds, for example, where and 2.7 days in Har. axyridis with smaller eggs (Osawa egg weight (E ) across species increases in direct pro- & Ohashi 2008 ). There is a strong selection pressure portion (almost isometrically) to body weight ( W ) on fast development and hatching synchrony in can- of the female and inversely to the ovariole number nibalistic ladybirds. Minimum egg size is, however, (O ): log E = 0.83 · log(W /O ) − 0.44 (Stewart et al. constrained by the minimum size at which fi rst instar 1991b ). larvae can fi nd (by extended walking) and kill prey The size of eggs is thus related to the average body (Stewart et al. 1991b ). size of the species; it is less than 0.4 mm in the smallest Small inter- individual variation in egg size was genera and over 2 mm in the largest genera. Eggs of reported in Har. axyridis: mean egg mass was 0.246 mg, Scymnus louisianae are 0.5 mm long and 0.2 mm wide with the minimum average in offspring of individual (Brown et al. 2003 ). Adult Clitostethus oculatus are females 0.196 and the maximum 0.278 (Prevolsek & only 1.26 mm long and the eggs are 0.41 mm long and Williams 2006 ). About 30 small eggs were laid com- 0.18 mm wide, greenish to yellowish- white, with a pared with only about 20 large eggs. Intra - individual reticulate chorion; whereas adult Delphastus pusillus variation in egg size with varying food levels was are 1.39 mm long, the eggs are 0.43 mm long and minimal. 0.23 mm wide, white and smooth (Liu & Stansly 1996a ). Eggs of Stethorus pusillus are 0.4 mm long, eggs of A. bipunctata 1.0 mm long, eggs of C. septem- 3.2.3 Cluster size punctata 1.3 mm long, eggs of Henosepilachna argus 1.7 mm long, and eggs of Anatis ocellata 2.0 mm long Eggs are either laid singly (Scymninae, Coccidulinae, (Klausnitzer & Klausnitzer 1986 ). Egg volume (V) in Chilocorinae – mostly coccidophagous groups) or in Life history and development 57 clusters ( batch , clutch – Coccinellinae – aphidopha- may have been underestimated, because some of them gous, Epilachninae – phytophagous) (Klausnitzer & had been emptied recently, therefore had not developed Klausnitzer 1986 ). There are a few exceptions. In a second large maturing oocyte, and thus were Chilocorinae, the coccidophagous Orcus chalybeus lay overlooked. eggs in clusters (Thompson 1951 ); Exochomus quadri- In interspecifi c comparisons, there is a general linear pustulatus usually lay their eggs in small groups but correlation between the number of ovarioles and the sometimes also individually (Sengonca & Arnold cluster size (Dixon & Guo 1993 ). However, adult size is 2003 ). Within Coccinellinae, Synonycha grandis lay strongly determined by food availability during previ- sparse clusters with the eggs a few millimetres apart; ous larval development (Rhamhalinghan 1985 ) while Megalocaria dilatata lay eggs in two rows (Iablokoff - cluster size is affected by food availability during the Khnzorian 1982 ). In the adelgid eating specialist development of oocytes. Oocyte development and Aphidecta obliterata , 20% of ‘ clusters ’ contain a single maturation takes a few days and there are several egg, and a maximum cluster size observed on spruce oocytes of different stages in each ovariole sequentially needles was fi ve eggs (Timms & Leather 2007 ). ordered in chambers or follicles, so that the female is The eggs in clusters of Coccinellinae are typically able to lay a full clutch of eggs from both ovaries daily. tightly packed in an upright position. The cluster size The total egg load is usually split into two or more is anatomically determined by the number of ovari- clusters. It is uncertain whether eggs of such small oles ( 3.5.5 ), which is similar in the left and right clusters come from one ovary only, or from a combina- ovaries. The usual number of eggs per cluster in tion of both. optimal conditions is equal to about half of the total Fois and colleagues (unpublished) found 5 – 72 eggs ovariole number. This may be because the female lays in clusters laid by a single female of Har. axyridis , the eggs from one of the two ovaries at a time. Stewart median and average being 28 eggs. This was a usual et al. (1991a) proposed that about half the ovarioles cluster size in this highly fertile species; well - fed young are active in egg production at any time, while the females laid two such clusters daily. However, the rest are preparing for new oviposition. This inter- number of eggs laid per day was often lower than the change of activity might enable more continuous total number of ovarioles of the female, which was egg production. The maximum number of eggs laid 53– 77 in this sample of Har. axyridis. The decrease in in one cluster in optimal conditions is close to the the number of eggs may have been due to suboptimal total number of ovarioles. However, dissections feeding with progressive ageing , and may vary with showed no signifi cant correlation between ovariole the frequency of mating. The average cluster weight number and egg cluster size in intraspecifi c data sets of Har. axyridis is 5.6 mg (21 eggs) (Prevolsek & Wil- of Har. axyridis and A. bipunctata (Ware et al. 2008 ; liams 2006 ). 5.2.3 ). The egg cluster size of Har. axyridis fed with eggs of Baungaard and H ä m ä l ä inen (1984) attest that the Ephestia kuehniella is 29 – 32 and 28 – 39. Females fed maximum cluster size is limited by the number with honey bee pollen oviposited only 8– 14 eggs per of ovarioles in a single ovary, since only one fully cluster, while those fed with the pea aphid, Acyrthosi- developed egg within an ovariole can be laid, and all phon pisum , laid 29 – 48 eggs per cluster (Berkvens et al. eggs in a cluster originate from the same ovary. They 2008a, b ). A larval diet of unlimited aphids resulted in suggested that larger clusters are a result of laying a the largest clusters of eggs being laid by the resulting second cluster in very close proximity to the fi rst one. Har. axyridis and A. bipunctata females (Ware et al. However, Majerus (1994) reported egg clusters which 2008 ), irrespective of the constant number of ovari- contained numbers well in excess of the maximum oles. For more examples on the effect of food on numbers of ovarioles recorded for the respective species cluster size see Table 3.1 . (C. septempunctata and A. bipunctata). He suggested that Egg cluster size is on average smaller (about 30 a cluster may include eggs from both ovaries , and versus 40 eggs) for a short photoperiod (12 h light) that more than one egg may be deposited from one than for a long one (16 h) in both the laboratory strain ovariole. Ware et al. (2008) reported egg clusters laid and wild population of the red succinea morph of Har. by an individual female that were bigger than the axyridis (Berkvens et al. 2008b ), while it is larger (34 number of ovarioles in both ovaries together. We versus 28) in the melanic morph. The average cluster suggest that the count of ovarioles during dissection size in a melanic colour morph of C. septempunctata 58 O. Nedveˇ d and A. Honeˇk
Table 3.1 Egg cluster size (C ), daily fecundity (D ) and lifetime fecundity (F ) of coccinellids. References for individual rows are numbered and listed below the table. C D F Prey, conditions Ref. Adalia bipunctata 11–17 — — — 8 11–16 (1 –47) — — — 10 — — 250 Aphis fabae 14 — — 676 Myzus persicae 14 11–14 — — — 15 15 (2 –43) — — — 25 —10—Myzus persicae on Brassica napus 28 —4 —Myzus persicae on Sinapis alba 28 —7 —Myzus persicae on Vicia faba 28 14 — — 34 — 9.3 738 Aphis fabae 35 — 20.4 max. 1535 Microlophium carnosum 35 15 (3 –25) — — — 37 — 12–20 — — 40 ——63 Aphis fabae 52 — — 1011 Phorodon humuli 52 14–28 — — Euceraphis betulae, 25 °C, 18L:6D 53 16–28 — — Eucallipterus tiliae, 25 °C, 18L:6D 53 14–24 — — Tuberculatus annulatus, 25 °C, 18L:6D 53 18–26 — — Liosomaphis berberidis, 25 °C, 18L:6D 53 14–22 — — Acyrthosiphon ignotum, 25 °C, 18L:6D 53 12–18 — — Macrosiphoniella artemisiae, 25 °C, 18L:6D 53 12–21 — — Cavariella konoi, 25°C, 18L:6D 53 12–21 — — Aphis fabae, 25 °C, 18L:6D 53 12–16 — — Aphis farinosa, 25 °C, 18L:6D 53 0——Aphis cirsiiacanthoidis, 25 °C, 18L:6D 53 0——Aphis spiraephaga, 25 °C, 18L:6D 53 — 16 537 Myzus persicae, 25 °C 63 — — 600 — 95 ——39 Acyrthosiphon caraganae 97 — — 264 Aphis pomi 97 — — 94, 241 Hyalopterus pruni 97 — — 161 Rhopalosiphum padi 97 30 — — — 108 31 20 — Acyrthosiphon pisum, 22 °C, 14L:10D, 30 115 days period; mean of individual maxima — 16.7 978 19°C 51 — 22.5 835 23°C 51 — 25.9 759 27°C 51 — 18.3 501 pollen + Ephestia kuehniella eggs 51 — 23.0 992 Acyrthosiphon pisum 51 — 23.7 1079 Myzus persicae 51 — 28.1 796 Acyrthosiphon pisum 122 — 33.3 1864 pollen + Ephestia kuehniella eggs 122 — 11.3 890 pollen + Artemia franciscana 122 — 6.3 265 pollen + lyophilized artifi cial diet 122 — 10.8 468 pollen + lyoph. art. diet + A. franciscana 122 Life history and development 59
Table 3.1 (Continued) C D F Prey, conditions Ref. Adalia decempunctata 11 — — — 21 Aiolocaria hexaspilota 26 (3 –74) — 881 (784 –1036) 47 Anatis ocellata — — 300 — 58 Anegleis cardoni — 6.8 397 Aphis gossypii, 27 °C, 14L:10D 84 — 6.3 328 Aphis craccivora, 27 °C, 14L:10D 84 — 5.1 137 Lipaphis pseudobrassicae, 27 °C, 14L:10D 84 Axinoscymnus cardilobus — — 125 17°C 43 — — 211 23°C 43 — — 20 32°C 43 Brumoides suturalis — — 142 Ferrisia virgata + Planococcus minor 29 — — 182 Ferrisia virgata 29 ——18 Phthorimaea operculella 29 — — 214 Planococcus minor 29 Callicaria superba — — 237 — 49 Calvia decemguttata — — 162–257 — 62 Calvia duodecimmaculata — — 165 Rhopalosiphum padi 62 — — 127 Aphis pomi 62 — — 193 Psylla mali 62 Calvia quatuordecimguttata — — 185 Psylla alni 62 — — 247 Psylla mali 62 — — 114–133 Rhopalosiphum padi 62 — — 122 (106 –142) Aphis pomi 98 — — 38 (28 –46) Hyalopterus pruni 98 — — 158 (147 –183) Psylla alni 98 — — 219 (198 –243) Psylla mali 98 18 (10 –27) — 142 (113 –168) Psylla ulmi 98 — — 114 (98 –128) Rhopalosiphum padi 98 Ceratomegilla undecimnotata — — 139 spring 47 — — 73 summer 47 — 20 — aphids 102 — 9–14 — Ephestia kuehniella eggs 102 30 — — — 108 (Continued) 60 O. Nedveˇ d and A. Honeˇk
Table 3.1 (Continued) C D F Prey, conditions Ref. Chilocorus bipustulatus — 4.2 529 Aspidiotus nerii 114 Chilocorus nigritus —3 —Aonidiella orientalis 3 ——24 Melanaspis glomerata 22 — — 370 Aulacaspis tegalensis 32 —5 —Aspidiotus nerii 36 — — 57–93 — 50 — — 151 Parlatoria blanchardi 72 — 3 564 Abgrallaspis cyanophylli, 20 °C 88 — 6 1361 Abgrallaspis cyanophylli, 24°C 89 — 8 1008 Abgrallaspis cyanophylli, 26°C 88 — 6 872 Abgrallaspis cyanophylli, 30°C 88 — 3.5 432 Aspidiotus nerii, 26 °C 88 ——81 Aonidiella aurantii, 27 °C 50 ——86 Diaspidiotus perniciosus, 27 °C 50 ——93 Aspidiotus desctructor, 27 °C 50 ——87 Aulacaspis tubercularis, 27 °C 50 ——72 Chrysomphalus aonidum, 27 °C 50 ——79 Hemberlesia lataniae, 27 °C 50 ——71 Lepidosaphes cornutus, 27 °C 50 ——79 Melanaspis glomerata, 27 °C 50 — — 194 Aonidiella aurantii, 26 °C 100 — — 483 Aspidiotus nerii, 26 °C 100 — — 151 Parlatoria blanchardii, 27 °C 72 — — 292 Aonidiella orientalis, 24 °C 3 ——57 Aonidimytilus albus, 27 °C 3 — — 121 Aspidiotus desctructor, 30 °C 9 — — 102 Hemberlesia lataniae, 30 °C 9 — — 136 Melanaspis glomerata, 30 °C 9 — — 370+ Aulacaspis tegalensis, 21 °C 32 Clitostethus arcuatus — — 181 Siphoninus phillyreae 125 Clitostethus oculatus —3 —Bemisia tabaci 64 — 0.6 52 20°C 92 — 1.0 81 26°C 92 — 0.7 33 31°C 92 Coccinella leonina transversalis 16 — — — 74 — — 915 Aphis craccivora 80 — 21 1400 lifetime mating 81 — 23 376 single mating 81 Coccinella novemnotata 18 11.9 302 Brevicoryne brassicae, 25 °C 24 Life history and development 61
Table 3.1 (Continued) C D F Prey, conditions Ref. Coccinella septempunctata 25 18 — 15mg Acyrthosiphon pisum daily 20 41 34 — Acyrthosiphon pisum ad libitum 20 17 12.3 201 Brevicoryne brassicae, 25 °C 24 34 — — in the laboratory, fi eld collected 120 36 — — fi eld observation 120 —19—20Acyrthosiphon pisum / day 26 —32—30Acyrthosiphon pisum / day 26 — 28 (23 –37) — 105 aphids / day 30 — 7 (3 –10) — 50 aphids / day 30 — — 514–719 aphids 41 — — 34–228 artifi cial diets 41 — — 283–1182 aphids, 12–27mg/day 46 — — 0.3–50 artifi cial diet, 4.5–9.1mg/day 46 — — 1428 (268 –2386) Acyrthosiphon pisum, 25 °C, 16L:8D 54 — — 1286 (218 –2291) Sitobion avenae, 25 °C, 16L:8D 54 — — 626 (98 –1528) Aphis fabae, 25 °C, 16L:8D 54 — — 683 (134 –1839) Aphis craccivora, 25 °C, 16L:8D 54 — — 893 Aphis spiraephila 62 — — 356 Rhopalosiphum padi 62 — — 759 Sitobion avenae 62 — — 513 Schizaphis graminum 62 — — 476 Aphis gossypii 62 — — 448 Aphis pomi 62 — — 1061 Aphis craccivora 79 — — 739 Aphis gossypii 79 — — 203 Aphis nerii 79 — — 1764 Lipaphis pseudobrassicae 79 — — 1199 Myzus persicae 79 — — 488 Uroleucon compositae 79 — — 1061 Aphis craccivora 80 — 25 1764 lifetime mating 81 — 13 298 single mating 81 — — 552 — 93 — — 668 — 93 — — 79–313 varied with parental age 105 — — 705 melanic female + melanic male 106 — — 396 typical female + typical male 106 50 — — — 108 — 814 — 110 33–44 — — — 111 22.4 287 Aphis gossypii, 25°C 118 15–84 718–1485 (max. 1953) Tashkent 119 — 27 — seasonal peak, alfalfa 127 Coccinella transversoguttata — 15 — seasonal peak, alfalfa 127 Coccinella trifasciata 10 — — — 108 (Continued) 62 O. Nedveˇ d and A. Honeˇk
Table 3.1 (Continued) C D F Prey, conditions Ref. Coccinella undecimpunctata 21 12.4 371 Brevicoryne brassicae, 25°C 24 — max. 40 85–135 Palestina 33 1–37 max. 89 451–746 Egypt 48 — — 742–983 Aphis craccivora, single mated 132 Coelophora biplagiata 20 — — — 99 Coelophora bissellata 10 — — — 74 Coelophora inaequalis 9—— — 74 Coelophora saucia — 26 (max. 51) 785 16L:8D 76 — 16 (max. 40) 478 24L:0D 76 — 10 (max. 39) 311 8L:16D 76 — 2–3 (max. 50) 230–1044 varied with light colour 76 — — 120 10s mating 83 — — 310 1min mating 83 — — 380 one hour mating 83 — — 393 Aphis craccivora, newly emerged female 126 — — 1980 Aphis craccivora, 20 days old female 126 — — 240 Aphis craccivora, 60 days old female 126 — — 1506 Aphis craccivora, 1 mating 129 — — 2192 Aphis craccivora, 20 matings 129 Coleomegilla maculata — 2.6–3.0 — pollen 23 —1 —Leptinotarsa decemlineata eggs 38 —4 —Myzus persicae 38 5–7 — — the fi rst clutch 67 — 6.2 — pollen + Ephestia kuehniella eggs 131 — 6.8 — maize pollen 131 Delphastus catalinae — 34 — — 103 Epilachna vigintisexpunctata 24–28 — — 94 Exochomus quadripustulatus — 2.6 91 Acyrthosiphon pisum 91 — 4.3 173 Dysaphis plantaginea 91 — 1–16 139 12/24°C 101 — 1–11 97 9/19°C 101 Life history and development 63
Table 3.1 (Continued) C D F Prey, conditions Ref. Harmonia axyridis — 5 257 Pectinophora gossypiella eggs 1 — 13 — single pair in container 2 — 1.6–8.8 — 10–40 females per container 2 — 15 715 fresh eggs of Sitotroga cerealella 2 — 13 607 frozen eggs of Sitotroga cerealella 2 — — 834 Aphis fabae 6 — — 1536 Diuraphis noxia 6 29–32 — — Ephestia eggs 11 8–14 — — pollen 11 29–48 — — Acyrthosiphon pisum 12 28–39 — — Ephestia eggs 12 27 — — — 21 28 (5–72) — — Acyrthosiphon pisum 27 — — 751 Aphis gossypii, 14.5 –18°C 39 — — 164 artifi cial diet 42 — 25 3819 Hyperomyzus carduellinus, 25 °C 44 — 14 945 Hyperomyzus carduellinus, 30 °C 44 — 27 2310 Myzus persicae, 25 °C 44 — 22 778 Myzus persicae, 30 °C 44 —16—Aphis gossypii 59 — 18 561 Myzus persicae, 25 °C 63 — — 400–800 6 weeks, 18 °C 65 — — 900–1300 6 weeks, 24 °C 65 — — 800–1100 6 weeks, 30°C 65 — — 719 Acyrthosiphon pisum, 27°C 69 20 — — Aphis spiraecola 85 21 — — — 90 26 — — Acyrthosiphon pisum 86 12–52 20 100–200 Hyalopterus pruni 96 — 23 — aphids 102 — 34–41 — Ephestia kuehniella eggs 102 30 27 (max. 78) 1642 (703 –2263) Aphis fabae 107 23 — — alfalfa 111 31 — — weeds 111 47 19 — Acyrthosiphon pisum, 22 °C, 14L:10D, 30 115 days period; mean of individual maxima 39 — 455 frozen Ephestia kuehniella eggs 121 — — 128 Aphis glycines susceptible soybean 68 ——22 Aphis glycines resistant soybean 68 — 10.3 — fl ightless strain, 36. generation 130 — 19.3 — control strain, 36. generation 130 — — 888 Ephestia kuehniella eggs 136 — — 823 Schizaphis graminum 136 Harmonia yedoensis 24 — 401 frozen Ephestia kuehniella eggs 121 (Continued) 64 O. Nedveˇ d and A. Honeˇk
Table 3.1 (Continued) C D F Prey, conditions Ref. Henosepilachna sumbana 21–32 — — — 94 Henosepilachna vigintioctopunctata 26 — — — 94 Hippodamia convergens — — max. 1550 — 47 19 — — — 116 — — 589–851 Aphis craccivora, single mated 132 Hippodamia tredecimpunctata 10–40 — 107–407 USA 47 — — 316 Aphis gossypii 62 — — 345 Aphis spiraephila 62 — — 158 Brevicorine brasicae 62 — — 452 Schizaphis graminum 62 — — 327–504 Sitobion avenae 62 Hippodamia variegata 19 10.6 276 Brevicoryne brassicae, 25 °C 24 — 21 842 Myzus persicae, 25 °C 63 20 — — — 108 11–20 — 960 (789 –1256) Dysaphis crataegi, 25 °C, 16L: 8D 61 Megalocaria dilatata 2 × 14 — — — 47 Menochilus sexmaculatus — — 861 multiple mating 13 — — 70 single mating 13 — 44 (peak) — after 10 matings 75 — 55 (peak) — after 20 matings 75 — 55 (peak) — after 5 matings 75 — — 1998 Aphis craccivora 80 — 32 1898 lifetime mating 81 — 24 1268 single mating 81 — 16–27 92–275 old females 82 — 16–33 214–555 old males 82 — 4–6 43–64 senescent males 82 — 22–30 767–1318 young females 82 — 23–30 1118–1464 young males 82 — — 110 1min mating 83 — — 40 10s mating 83 — — 620 one hour mating 83 — 17.2 — Aphis craccivora, 15L:9D, 18 °C 109 — 9.9 — Aphis gossypii, 15L:9D, 18 °C 109 — — max. 2388 — 47 12 — — — 74 Micraspis discolor — — 385 20°C 77 — — 563 25°C 77 — — 750 27°C 77 — — 622 30°C 77 Life history and development 65
Table 3.1 (Continued) C D F Prey, conditions Ref. Nephus reunioni — 2.6 (max.) 177 Planococcus citri, 25°C 134 Nephus includens — — 151 — 135 Oenopia conglobata 5—— — 21 8–15 — — — 47 — — 439 Aphis spiraephila 62 — — 643 Rhopalosiphum padi 62 — — 327 Aphis pomi 62 — — 349–453 Central Asia 119 Oenopia lyncea — — 40 — 117 Olla v-nigrum 27 — — — 108 17 5.7 72 Acyrthosiphon pisum, 15 °C, 12L:12D 137 13 8.1 200 Acyrthosiphon pisum, 20 °C, 12L:12D 137 13 12.4 269 Acyrthosiphon pisum, 25 °C, 12L:12D 137 14 6.4 329 Acyrthosiphon pisum, 20 °C, 18L:6D 137 Propylea dissecta — — 150 interference with 4 females 71 — — 336 single female 71 — 37 (peak) — after 10 matings 75 — 19 (peak) — after 20 matings 75 — 33 (peak) — after 5 matings 75 — — 278–710 1 to multiple matings 78 — — 942 Aphis craccivora 80 — — 867 20 day old females after single mating 87 Propylea japonica — — 644 — 47 7–9 — — — 56 Propylea quatuordecimpunctata 1–24 20 (max. 65) 1308 (max. 1800) England, laboratory 47 10 — fi eld collected in laboratory 120 6.4 — fi eld 120 — — 386 Myzus persicae on Bt potatoes 55 — — 345 Myzus persicae on non -Bt potatoes 55 — — 278 Aphis craccivora 55 — — 431 Aphis craccivora + Myzus persicae on Bt 55 potatoes — — 119 Aphis gossypii 62 — — 351 Sitobion avenae 62 — — 211 Aphis spiraephila 62 12 — — — 108 (Continued) 66 O. Nedveˇ d and A. Honeˇk
Table 3.1 (Continued) C D F Prey, conditions Ref. Propylea quatuordecimpunctata × Propylea japonica — — 149 — 47 Psyllobora confl uens — 17 440 Erysiphe cichoracearum 18 Sasajiscymnus tsugae — 2.9 280 (max. 513) Adelges tsugae, 25°C 45 Scymnus frontalis — — 151 22°C 31 — 7.3 — Diuraphis noxia, 26 °C 73 Scymnus hoffmanni — — 127 25°C 57 Scymnus interruptus — — 88 20°C 133 — — 402 24°C 133 Scymnus levaillanti — 4.9 428 20°C 113 — 5.9 456 25°C 113 — 8.3 393 30°C 113 — 2.6 83 35°C 113 Scymnus louisianae — — 122 Aphis glycines, 23 °C, 15:9 L :D 16 Scymnus marginicollis — — 75 20–25°C 17 Scymnus marinus — — 1.7 15°C 70 — — 602 30°C 70 Scymnus sinuanodulus — 2.5 130 (max. 200) 66 Scymnus subvillosus ——99 Hyalopterus pruni, 5 aphids. per day 7 — — 232 Hyalopterus pruni, 80 aphids per day 7 Scymnus syriacus — — 588 Aphis spiraecola on Citrus sinensis 104 — — 658 Aphis spiraecola on Spirea sp. 104 Serangium parcesetosum ——28 Trialeurodes vaporariorum 5 Serangium japonicum — — 387 Bemisia tabaci, 20°C 124 Stethorus bifi dus — 1 2–33 10 mites / day 19 — 2 24–67 20 mites / day 19 — 6 308–438 50 mites / day 19 Life history and development 67
Table 3.1 (Continued) C D F Prey, conditions Ref. Stethorus gilvifrons — 4.4 149 Oligonychus coffeae 123 Stethorus japonicus — 8.1 — Amphitetranychus viennensis, 27 °C: 60 16L8D — 5.4 — Panonychus mori, 27 °C: 16L:8D 60 — 7.1 — Tetranychus urticae, 27 °C: 16L:8D 60 Stethorus pussilus — — 54–60 — 4 — — 122 Bt-maize 128 — — 111 non-Bt-maize 128 Subcoccinella vigintiquatuorpunctata — — 200–300 — 112 Synonycha grandis 3–60 — 360 — 47
1, Abdel-Salam et al. 1997; 2, Abdel-Salam and Abdel-Baky 2001; 3, Ahmad 1970; 4, Alvarez-Alfageme et al. 2008; 5, Al-Zyoud et al. 2005; 6, Anonymous 1997; 7, Atlıhan and Güldal 2009; 8, Banks 1955, 1956 ; 9, Baskaran and Suresh 2006; 10, Baungaard and H ämäläinen 1981; 11, Berkvens et al., 2008a; 12, Berkvens et al., 2008b; 13, Bind 2007; 14, Blackman 1965; 15, Blackman 1967; 16, Brown et al. 2003; 17, Buntin and Tamaki 1980; 18, Cividanes et al. 2007; 19, Collyer 1964; 20, Dixon and Guo 1993; 21, Dobzhansky 1924; 22, Dorge et al. 1972; 23, Duan et al. 2002; 24, ElHag and Zaitoon 1996; 25, Ellingsen 1969; 26, Evans et al. 2004; 27, Fois and Nedve ˇ d, unpublished; 28, Francis et al. 2001; 29, Gautam 1990; 30, Ghanim et al. 1984; 31, Gibson et al. 1992; 32, Greathead and Pope 1977; 33, Hafez in Iablokoff- Khnzorian 1982; 34, H ämäläinen and Markkula 1977; 35, Hariri 1966; 36, Hattingh and Samways 1994; 37, Hawkes 1920; 38, Hazzard and Ferro 1991; 39, He et al. 1994; 40, Hemptinne et al. 1992; 41, Hodek 1996a; 42, Hong and Park 1996; 43, Huang et al. 2008; 44, Hukushima and Kamei 1970; 45, Cheah and McClure 1998; 46, Chen et al. 1980; 47, Iablokoff-Khnzorian 1982; 48, Ibrahim 1955; 49, Iwata 1932; 50, Jalali and Singh 1989; 51, Jalali et al. 2009; 52, Kalush- kov 1994; 53, Kalushkov 1998; 54, Kalushkov and Hodek 2004; 55, Kalushkov and Hodek 2005; 56, Kawauchi 1981; 57, Kawauchi 1985; 58, Kesten 1969; 59, Kim and Choi (1985); 60, Kishimoto 2003; 61, Kontodimas and Stathas 2005; 62, Kuznetsov 1975; 63, Lanzoni et al. 2004; 64, Liu et al. 1997; 65, Lombaert et al. 2008; 66, Lu and Montgomery 2001; 67, Lundgren and Wiedenmann 2002; 68, Lundgren et al. 2009; 69, McClure (1987); 70, M ’Hamed and Chemsed- dine 2001; 71, Mishra and Omkar 2006; 72, Muralidharan 1994; 73, Naranjo et al. 1990; 74, Ng 1986; 75, Omkar and Mishra 2005b; 76, Omkar and Pathak 2006; 77, Omkar and Pervez 2002; 78, Omkar and Pervez 2005; 79, Omkar and Srivastava 2003; 80, Omkar et al. 2005a; 81, Omkar et al. 2005b; 82, Omkar et al. 2006b; 83, Omkar et al. 2006a; 84, Omkar et al. 2009; 85, Osawa 2005; 86, Perry and Roitberg 2005; 87, Pervez et al. 2004; 88, Ponsonby 2009; 89, Ponsonby and Copland 1998; 90, Prevolsek and Williams 2006; 91, Radwan and Lovei 1983; 92, Ren et al. 2002; 93, Rhamhalinghan 1986; 94, Richards and Filewood 1988; 95, Savoiskaya 1965; 96, Savoiskaya 1970; 97, Semyanov 1970; 98, Semyanov 1980; 99, Semyanov and Bereznaya 1988; 100, Senal 2006; 101, Sengonca and Arnold 2003; 102, Schanderl et al. 1988; 103, Simmons et al. 2008; 104, Soroushmehr et al. 2008; 105, Srivastava and Omkar 2004; 106, Srivastava and Omkar 2005; 107, Stathas et al. 2001; 108, Stewart et al. 1991b; 109, Sugiura and Takada 1998; 110, Sundby 1968; 111, Takahashi 1987; 112, Tanasijevic 1958; 113, Uygun and Atlıhan 2000; 114, Uygun and Elekcioglu 1998; 115, Ware et al. 2008; 116, Williams 1945; 117, Witsack 1971; 118, Xia et al. 1999; 119, Yakhontov 1958; 120 Honeˇ k et al. 2008; 121, Osawa and Ohashi 2008, 122, Bonte et al. 2010, 123, Perumalsamy et al. 2010, 124, Yao et al. 2010, 125, Tavadjoh et al. 2010, 126, Omkar et al. 2010b, 127, Kajita and Evans 2010, 128, Li and Romeis 2010, 129, Omkar et al. 2010a, 130, Seko and Miura 2009, 131, Pilorget et al. 2010, 132, El -Heneidy et al. 2008, 133, Tawfi k et al 1973, 134, Izhevsky and Orlinsky 1988, 135, Transfaglia and Viggiani 1972, 136, dos Santo et al. 2009, 137, Kreiter 1985. 68 O. Nedveˇ d and A. Honeˇk in India was 8.9 eggs, while the same in typical morphs of lifetime fecundity (Fig. 3.2 ; Omkar & Srivastava was 14.34 (Rhamhalinghan 1999 ). 2003 ). Hatching rate varied with temperature in Har. axyridis . Between 18 and 24 ° C, the rate was 65 – 90%. At 30 ° C, it decreased to 30 – 65% (Lombaert et al. 3.2.4 Hatching rate 2008 ). The highest temperature, 30 ° C, was lethal for most eggs of a population from the Czech Republic, The percentage of eggs in a cluster that develop fully regardless of humidity (O. Nedve ˇd, unpublished). In and from which larvae eventually hatch is called Micraspis discolor in India, the egg hatch rate was hatching rate, egg viability , or percentage fertility lowest (65%) at the lowest experimental temperature (100– progeny loss). It is often substantially less than (20° C), highest (95%) at optimum temperature (27° C), 100%. The hatching rate differentiates fecundity and decreased (83%) at the highest temperature (30° C) (number of eggs per female) from fertility (number of (Omkar & Pervez 2002 ). viable progeny per female). High humidity is favourable for embryonic develop- Some eggs are non- fertile due to low sperm volume ment and larval hatching; 99% of the eggs of Delphas- and quality. Other eggs are fertilized but do not tus catalinae hatched at 85% RH, while 85% hatched at develop or fail to hatch due to infection by various 25% RH (Simmons et al. 2008 ). bacteria. In most species of invertebrates, male- There was no consistent difference in the hatching killing occurs during embryonic stages (early male- rate of Har. axyridis at long (16L:8D) and short killing) and is associated with cytoplasmic bacteria, (12L:12D) photoperiod s (Berkvens et al. 2008b ). including Wolbachia , Spiroplasma , Rickettsia , Flavobacte- Wild populations hatched better than the laboratory rium and gamma proteobacteria (Nakanishi et al. strain. Nor in Coelophora saucia was the hatching 2008 ; Chapter 8 ). These bacteria kill only, or mostly, rate very different (92– 97%) under different photope- male embryos, giving a hatching rate close to 50%. The riods or under continuous light (Omkar & Pathak female larvae of ladybirds, especially Coccinellinae, i.e. 2006 ). the sisters of the killed males, have a nutritive advan- Hatching rate was high (76 – 90%) when the eggs of tage over the females from uninfected clusters, because Menochilus sexmaculatus were fertilized by young males they cannibalize those undeveloped ‘ male ’ eggs (4 – 50 days), and low (12 – 25%) when fertilized by old (Majerus 1994 ). males (60– 110 days) (Omkar et al. 2006b ). A similar Most authors do not discriminate between ‘ non - pattern was found in C. septempunctata (Srivastava & fertile ’ and ‘ non - developing ’ eggs and record the pro- Omkar 2004 ). Hatching rate of A. bipunctata remained portion of hatched eggs. Under optimal conditions this high (80– 90%) for 1 or 2 months old males and then is high: 100% eggs of C. septempunctata and C. leonina decreased to 20 – 30% (Jalali et al. 2009a ) and that of transversalis fed with Lipaphis pseudobrassicae , Myzus Anegleis cardoni increased from almost zero to more persicae or Aphis nerii hatched (Gupta et al. 2006 ). than 80% at a female age of 2 weeks (Omkar et al. There were 6% unhatched eggs in P. quatuordecimpunc- 2009 ). tata in England in the fi eld (Banks 1956 ). They were Multiple matings enhanced the total egg output consumed by newly born larvae. Laboratory progeny and the percentage of hatching (Kesten 1969 , Semy- loss ranged from 5% in C. leonina transversalis , 6% in anov 1970 , Omkar & Pervez 2005 , Bind 2007 ). Hatch- P. dissecta , through 10% in Menochilus sexmaculatus ing rate gradually decreased to 50% after the female of to 25% in C. septempunctata (Omkar et al. 2005 ) when P. dissecta has been separated from the male (Omkar & the ladybirds were reared on a suboptimal prey , Mishra 2005 ). However, the hatching rate was high Aphis craccivora . In A. bipunctata fed with optimal in Menochilus sexmaculatus , C. septempunctata and C. prey, Myzus persicae , the hatching rate was 89%, asso- leonina transversalis even when females mated only ciated with high fecundity (676 eggs per female), once (Omkar et al. 2005b ). The level of crowding had while both measures decreased on a suboptimal prey, a small detrimental effect on egg viability of P. dissecta Aphis fabae (56%, 250 eggs; Blackman 1965 ). The (Mishra & Omkar 2006 ). decrease of hatching rate of C. septempunctata among To describe hatching synchrony in individual six prey species was clearly correlated with a decrease species, three indices have been proposed (Perry & Life history and development 69
100
90
80
70
Hatch rate [%] 60
50
40 0 500 1000 1500 2000 Fecundity [eggs]
Figure 3.2 Relationship between average egg hatching rate (%) and lifetime female fecundity (eggs). The parallel increase in both parameters in Coccinella septempunctata (dots, lower line) was recorded simultaneously when six prey species were offered (after Omkar & Srivastava 2003 ). The increase in Coelophora saucia (diamonds, upper line) was recorded at (from the left) red, blue, yellow, and white light (after Omkar & Pathak 2006 ). Trend lines plotted as power functions.
Roitberg 2005 ): (i) total hatch time, related to batch hatched during the night (Mishra & Omkar 2004 ; size; (ii) the average interval between two sequential Fig. 3.3 ). hatching larvae; (iii) the proportion of eggs per cluster, weighted by cluster size, that are vulnerable to sibling 3.2.5 Trophic eggs cannibalism by hatching later than the quiescent period of the fi rst larva (141 min). The total duration Apart from viable hatching eggs, ladybirds also produce of hatching of the fi rst instar larva from an egg lasted non - hatching eggs, which may be either infertile (not 1 to 3.5 hours in Har. axyridis , and the total hatch time fertilized by sperm) or non- viable, where an embryo of the whole cluster (i) ranged from 61 to 203 minutes develops for some time but the larva does not emerge (Perry & Roitberg 2005 ). Hatching was synchronized from the egg capsule. Non - hatching eggs are some- within a cluster; the interval between hatching of suc- times considered as trophic eggs that serve as the fi rst cessive larvae (ii) was 7– 15 minutes. The proportion of food for the newly born sibling larvae. Egg cannibal- eggs which showed a delayed hatch (iii) ranged from 0 ism ( 5.2 , Chapter 8 ) is undoubtedly advantageous to to 7%. A. bipunctata larvae both in terms of faster develop- The mean duration of hatching of larvae within the ment and increased survival (Roy et al. 2007 ). Perry same batch (i) ranged between 1.01 hours in Coelo- and Roitberg (2005) showed that laying infertile eggs phora inaequalis and 1.36 hours in C. leonina transver- is also an active part of the maternal strategy in Har. salis (Ng 1986 ). There were 45% (Coelophora inaequalis ) axyridis . Females produced 56% more infertile eggs (23 to 83% ( C. leonina transversalis) egg clusters which took versus 15% of the cluster) in low versus high food longer to hatch than the duration between emergence treatments; they manipulated the proportion of trophic of a larva and its cannibalization of eggs (a similar eggs in favour of young fi rst instar larvae that might measure to (iii)). have problems in fi nding essential prey (aphids). The Although hatching of ladybird larvae often occurs oviposition sequence of infertile eggs within a cluster in daytime, most egg clusters (73%) of P. dissecta did not differ from random. 400 400 Mating Oviposition 350 350
300 300
250 250
200 200
150 150 Incidence per day [%] day per Incidence 100 100
50 50
0 0 0612182406121824 Time intervals [h from light on] Time intervals [h from light on]
400 400 Hatching Moulting 350 350
300 300
250 250
200 200
150 150 Incidence per day [%] day per Incidence 100 100
50 50
0 0 0612182406121824 Time intervals [h from light on] Time intervals [h from light on]
400 400 Pupation Eclosion 350 350
300 300
250 250
200 200
150 150 Incidence per day [%] day per Incidence 100 100
50 50
0 0 0612182406121824 Time intervals [h from light on] Time intervals [h from light on]
Figure 3.3 Circadian rhytmicity in life events of aphidophagous ladybird beetles (Coccinellini) in India. Dashed line and solid circles, Menochilus sexmaculatus (Omkar & Singh 2007 ); dotted line and open circles, Propylea dissecta (Mishra & Omkar 2004 ); dotted line and diagonal crosses, Coccinella septempunctata; dotted line and straight crosses: Coccinella transversalis; dotted line and triangles, Propylea dissecta (all three Omkar et al. 2004 ). Photophase: 0– 12 h, scotophase: 12– 24 h. All values are expressed in relative incidence, mean is 100%. Mating occurs more frequently around sunrise and around sunset; oviposition take place mainly during scotophase with two peaks (beginning and late scotophase); hatching from eggs occurs mainly during the second half of scotophase; larval moulting is more regularly distributed, with slight prevalence in scotophase; pupation occurs mainly during early or mid scotophase; adult emergence take place either during morning or during the second half of scotophase. Life history and development 71
3.3 LARVA which use chewing and sucking (Isikber & Copland 2001 ). 3.3.1 Larval morphology The legs are elongate in the Epilachninae and Coccinellinae, but shorter in the Scymninae. The Larvae of most coccinellid tribes have an elongate antennae are very short, 1 – 3 segmented; the fi rst body (Coccinellinae, Scymnini). It is ellipsoidal in the segment is short and wide (Savoiskaya & Klausnitzer Hyperaspidini and Noviini and hemispherical in the 1973 ). Platynaspidini. The pronotum has two or four sclero- tized plates (six in Tetrabrachys ; Klausnitzer 1969a ). The meso - and metanotum each have two plates, 3.3.2 Instars but in the Scymninae they are weakly developed or absent. The fi rst eight abdominal segments bear six The individual substages during larval development rows of characteristic structures as dorsal, dorsola- separated by moulting (ecdysis) are called instars. The teral and lateral pairs. These structures are well devel- number of instars in the whole family is almost always oped in the third and fourth instars and differ according four, independent of the species size, developmental to their shape, with seven types: seta, chalaza, tuber- conditions, etc. The constant and same number of cule, struma, parascolus, sentus and scolus (Gage instars in both aphidophagous and coccidophagous 1920 ). These structures are important in taxonomy ladybirds, otherwise strongly different in many life and identifi cation. Larvae of Hyperaspidini and Platy- history characteristics, was considered surprising by naspidini are covered by chalazae and setae, the Dixon (2000) . Fast development, typical and adaptive Scymnini and Noviini have tubercules, the Psyllo- for aphidophagous Coccinellinae, would be better borini and Tytthaspidini strumae, the Chilocorini achieved by fewer instars, but their number seems to senti and the Epilachninae scoli. Genera of Coccinellini be phylogenetically constrained. have variable structures (Savoiskaya & Klausnitzer The last, fourth, instar eventually stops feeding and 1973 ). The more elaborate structures have a defensive attaches to a substrate, forming the so- called prepupa. role. This pseudostage has sometimes been erroneously Larvae of most Scymninae, Telsimiini and Azyini referred to as a fi fth instar (Smith et al. 1999 ). Three (including Cryptolaemus ) are covered with a white instars were surprisingly reported in the coccidopha- waxy exudation (fi laments) as a defensive adaptation gous Hyperaspis campestris (McKenzie 1932 ) and in an (Liere & Perfect 2008 ). Many larvae exhibit defensive Egyptian population of C. undecimpunctata (while Euro- refl ex bleeding similar to that of adults, but the droplets pean populations of this species have four (Iablokoff- exude from specifi c sutures or structures on the Khnzorian 1982 )). Four larval instars were usually abdomen or thorax. Larvae of Scymnus sinuanodulus observed in Clitostethus oculatus , although a signifi cant exhibit refl ex bleeding of orange viscous droplets from proportion of third instar larvae moulted directly to thoracic tubercles (Lu et al. 2002 ). Larvae of third and the pupal stage at 29 ° C or above (Ren et al. 2002 ). For fourth instars, namely of Coccinellinae, are brightly these latter individuals, the third larval instar was pro- coloured. longed to almost the length of the combined third and The mandibles of larvae in the Hyperaspiidini, fourth instars of ‘ normal ’ beetles (6.1 days versus 6.3 Platynaspidini, Stethorini, Scymnini and Exochomus days at 29 ° C, 3.4 days versus 4.9 days at 31 ° C and 4.7 have an apex ending with a single point; they have two days versus 5.0 days at 33° C). apical teeth in the Coccinellini, Noviini and also in the However, a true higher number of instars, fi ve, was larvae of Chilocorus , though in this genus the adults reported for Callicaria superba (Iwata 1932 ), a large possess a mandible terminating in only a single point. ladybird (12 mm) which feeds on Sternorrhyncha, In the phytophagous Epilachninae, mandibles are Auchenorrhyncha and chrysomelid larvae. There is equipped with four or fi ve large teeth. There is a row of also a report of fi ve larval instars in Chil. nigritus (Fit- smaller teeth or thick setae in the mycophagous Psyl- zgerald 1953 , Chazeau 1981 ), a species feeding on loborini and Tytthaspidini (Savoiskaya & Klausnitzer coccids, aphids and whitefl ies (Omkar & Pervez 2003 ). 1973 ). The larvae of Scymnus levaillanti, which employ A small proportion of larvae of Col. maculata (Warren pre- oral digestion, were more effi cient in converting & Tadi c´ 1967 ) and Chil. bipustulatus (Yinon 1969 ) food to body mass than larvae of Cycloneda sanguinea , went through fi ve instars in the laboratory. 72 O. Nedveˇ d and A. Honeˇk
0.10
0.08
0.06 -value k 0.04
0.02
0.00 e1234ppp Stage
Figure 3.4. Stage specifi c mortality ( k - values = log10 ax − log10 ax+ 1 , where a x is the initial number of individuals and a x+1 is the number of individuals surviving to the next stage) of Propylea dissecta. Average for fi ve generations reared on fi ve different aphid species. The fi rst instar and eggs are most vulnerable to death, prepupa is the most resistant ‘ stage ’ (after Omkar & Pervez 2004 ).
A fi fth larval instar occurred in 33% of the individu- ( 3.6 ), and also on the quality and quantity of food als of a Canadian population of the large invasive ( 5.2 ). aphidophagous Har. axyridis. This extra instar had the Larval development of coccinellids is direct with no same developmental time as ordinary fourth instars, diapause. An exception is the fourth instar of the phy- but showed increased voracity and weight gain com- tophagous Epilachna admirabilis which is sensitive to pared to the fourth larval instar, suggesting an photoperiod (Takeuchi et al. 1999 ). The fourth instar increased fi tness of those individuals and contributing larvae of Scymnus abietis have been observed very early to the invasiveness of the species (Labrie et al. 2006 ). in the spring, suggesting that they overwinter in this A fi fth instar was found to occur rarely also in Euro- stage (Nedve ˇ d & Kov á rˇ , unpublished). pean population of Har. axyridis at 20 ° C with an excess In well- fed larvae, the fi rst instar takes about 24% of of food. Only females developed from these larvae the total developmental time, the second 17%, the (Ungerov á , unpublished). third 19% and the fourth 40% (Hone ˇ k 1996 ). There Moulting between instars occurs at any time of day, was higher variation in these percentages in A. bipunc- although in P. dissecta 61– 77% of larvae moulted tata (Obrycki & Tauber 1981 ) than in Col. maculata during the scotophase (Mishra & Omkar 2004 ). (Wright & Laing 1978 ). Even when the prepupa (8 – During pre - adult development, mortality is highest 11%) is not included, the last instar is always longer in the fi rst instar, possibly higher than in eggs, is least than any of the others. in prepupae and increases somewhat during the pupal Immune responses to microbial infection may cause stage (Fig. 3.4 ; Omkar & Pervez 2004b ). developmental delay. The mean larval duration of Serangium parcesetosum was longest (22.5 days) when sprayed with medium and high dosages of Beauveria 3.3.3 Development bassiana, intermediate (20 days) with a low dosage of B. bassiana, and lowest (18 days) for the blank control The duration of larval development is species specifi c and the Paecilomyces fumosoroseus treatments (Popraw- and strongly dependent on the ambient temperature ski et al. 1998 ). B. bassiana strain ATCC 44860 Life history and development 73 increased the development time of Col. maculata fed Weight increases again in adults once they start to feed with Colorado potato beetle larvae, whereas the strain after emergence (Omkar et al. 2005a ). The size of ARSEF 2991 reduced the development time (Todorova cuticular structures of successive instars increases in et al. 1996 ). constant proportions. Weight increases exponentially, Development of phytophagous species may depend e.g. in A. bipunctata it is 0.04, 0.17, 0.52, 1.51 and not only on the quality but also on the surface struc- 4.85 mg at the beginning of the fi rst, second, third and ture of the host plant. Larvae of the Mexican bean fourth instar and prepupa, respectively (Jalali et al. beetle, Epilachna varivestis , completed the fi rst instar 2009b ). most quickly on pubescent soybean plants, whereas The fi nal size of the ladybird is largely determined the duration of the third instar was shortest on gla- during the fourth instar (Hon eˇ k 1996 ). For compara- brous plants. Larval mortality was 2.5 – 5 times greater tive purposes, the mean relative growth rate (RGR) on a densely pubescent isoline than on glabrous and may be calculated as RGR = dry weight gained during normal soybean isolines (Gannon & Bach 1996 ). the feeding period / (length of feeding period in days · The duration of pre - imaginal development differed mean dry weight of predator during feeding period) among several isofemale lines (progeny of individual (Waldbauer 1964 ). RGR values in A. bipunctata females, from several egg batches) of fi eld - collected fed with Myzus persicae were 0.45, 0.70, 0.55 and Hip. convergens , the values ranging from 223 to 273 0.35 per day in the successive instars (Jalali et al. degree days above the lower temperature threshold 2009b ). (Rodriguez - Saona & Miller 1999 ). Accordingly it is rec- The relative food consumption of different larval ommended that experiments on the effects of environ- instars is compared in 5.2. For example, Okrouhla mental factors on coccinellids should be (i) conducted et al. (1983) gave average values of 6, 11, 21 and with siblings (the progeny of one female) distributed 62% for the total food eaten by larvae of Cheilomenes into all treatments and (ii) repeated with the progeny sulphurea. In A. bipunctata, the percentages of food of several unrelated females. eaten by the four larval instars differed between The duration of larval development further depends food treatments. When fed with aphid Myzus persicae, on population density . In Chil. bipustulatus, duration they were 4, 9, 14 and 73% and with factitious food of development increased at higher density (Fomenko (a mixture of Ephestia kuehniella eggs and fresh 1970 ). Rearing P. dissecta larvae at a moderate density bee pollen) they were 5, 8, 20 and 67% (Jalali et al. of four larvae in a half litre beaker shortened develop- 2009b ). mental time and increased immature survival when compared with both single larvae and higher densities of larvae (Omkar & Pathak 2009 ). Mean developmen- 3.4 PUPA tal time of Har. axyridis in small (7 cm) Petri dishes was 13.7 days; in 15 cm Petri dishes it was 11.5 days; and 3.4.1 Prepupal stage 11.7 days in 0.5 l jars (Ungerov á et al. 2010 ). The effect of diverse environmental conditions on The last (fourth) instar larva attaches itself by the tip development may be mediated through the quality of of its abdomen ( ‘ anal organ ’ , pygopod) to the substrate prey. Duration of larval development of P. japonica was and prepares for pupation. The prepupae of particular signifi cantly longer if fed Aphis gossypii from cotton species are as or more vulnerable to predation than grown at elevated than at normal CO2 concentrations their fourth instar larvae. Their physical defence struc- (Gao et al. 2008 ). tures are essentially the same, but they are practically immobile (Ware & Majerus 2008 ). Phorids attack host prepupae and parasitize them at the time of 3.3.4 Body size ecdysis to the pupal stage (Hurst et al. 1998 ). In life tables, the prepupa is often listed as one of the develop- When fed ad libitum , the body mass increases exponen- mental stages, but strictly speaking it should be consid- tially with the age of the larva, peaking in the late last ered as a part of the last instar larva . For practical instar larva. Due to the cessation of further weight reasons, especially the differences between feeding gain at the end of the last larval instar (Ng 1991 ) the larva and inactive prepupae, we recommend that these function of weight increase is sigmoid (Fig. 3.5 ). substages are separated in experiments. 74 O. Nedveˇ d and A. Honeˇk
16 pp i 14 p
12
10 l4
8
Mass [mg] Mass 6 l3
4 l2 2 l1 e 0 0 5 10 15 20 Age [days]
Figure 3.5 Growth curves of ladybirds. Crosses, growth of Exochomus quadripustulatus from egg to pupa at 25° C, fed with Pulvinaria regalis (after Sengonca & Arnold 2003 ). Circles, growth of Coelophora biplagiata from egg (e) through four larval instars (i), prepupa (pp), pupa (p) to adult (a); reared on Aphis craccivora at 27° C (after Omkar et al. 2005 , mass was in fact double, but the values were reduced to a similar scale as the other species). Body mass increases exponentially from hatching to the fourth instar. This last instar stops to feed and grow and form a prepupa. The pupa is lighter than prepupa because the larval cuticle is shed, and some of the nutrients are spent through intensive metabolism. Part of the body water may be lost during the resting stage. Adults continue to grow, especially the females during egg production.
3.4.2 Pupal morphology The size of the pupa of particular species is highly dependent on prey quality and quantity during larval Pupae of coccinellids are of the type pupa adectica development, as well as on the temperature during obtecta , which means that all appendages (antennae, development. The largest pupae develop at medium limbs, wing pads) are glued to the body by exuvial fl uid. temperatures. The mean weight of pupae of Exo- The pupa is attached to the substrate (vegetation) by chomus quadripustulatus was 11.9 mg at 9/19 ° C (ther- the tip of the abdomen. The exuviae (remains of the moperiod), 12.5 mg at 12/24 ° C and 10.7 mg at a old cuticle) of the last larval instar are crumpled constant 25 ° C (Sengonca & Arnold 2003 ). The heavi- around the tip of abdomen in the Coccinellinae and est pupae of Hip. convergens were reared at 22 ° C as Sticholotidinae. In the Chilocorinae, Scymninae and compared with 18, 26 and 30 ° C (Rodriguez - Saona & Ortaliinae the larval cuticle ruptures on the dorsal side, Miller 1999 ). stretches and splits lengthwise, but is not shed and Har. axyridis larvae reared on Acyrthosiphon pisum forms a protective chamber around the pupa. There produced heavier pupae (27.8 mg) than their siblings are exceptions such as Scymnus sinuanodulus where the reared on the less suitable prey Aphis craccivora pupa is naked with the larval exuviae attached only (20.8 mg) or on artifi cial diet (22.0 mg) (Ueno 2003 ). to the last abdominal segment (Lu et al. 2002 ). In the Coleomegilla maculata larvae fed with corn pollen gave Epilachninae, only the posterior third of the pupa is much heavier pupae (13 mg) than individuals fed on covered by the spiny larval exuviae. The pupal cuticle the aphid Rhopalosiphum padi (7.3 mg) (Lundgren & itself is either covered in long hairs (Epilachninae, Wiedenmann 2002 ). Epilachna varivestis reared on gla- Scymninae) or is apparently smooth, with only sparse brous soybean plants had by 14 – 29% greater dry very short glandular hairs (Coccinellinae). pupal weights than did individuals reared on the Life history and development 75 densely pubescent and normal isolines (Gannon & where 0 hours is the time the light was switched on) Bach 1996 ). and early scotophase (12:00 – 15:00 hours) in Meno- Male and female pupae cannot be distinguished by chilus sexmaculatus (Omkar & Singh 2007 ; Fig. 3.3 ). their external morphology. Females tend to be larger Mass - specifi c respiration rates in Har. axyridis and heavier than males in the pupal stage: Har. axyridis increased with increases in pupal age (while it females on average weighed 28.5 mg while males were decreased in the other stages) (Acar et al. 2004 ). Below
27.2 mg (Ueno 2003 ). Moreover, Ueno (2003 ) found 10 ° C, CO 2 was produced primarily from non- oxygen - slight intraspecifi c genetic variation ( family effect ) consuming reactions. CO2 production gradually shifted in pupal weights and an interaction of this genetic more to oxygen- consuming reactions with increasing background with the type of prey. Based on these temperature. fi nding we suggest (i) strict use of siblings in all treat- The abundance of pupae is widely underestimated ments of an experiment where effects of several envi- in the fi eld because they are attached to the vegetation ronmental factors are to be studied, and (ii) the parallel and thus unavailable for common sampling methods use of several unrelated females/families for such (sweeping, Kalushkov & Nedv eˇ d 2005 ; beating, Kula experiments. & Nedv eˇ d unpublished; sticky traps, Kaneko et al. 2006 ).
3.4.3 Timing of pupation 3.4.4 Places of pupation The development of pupae generally takes about 24% of the total pre - imaginal development time, i.e. less The usual place for pupation is on the vegetation where than in other Aphidophaga (Neuroptera: 33%, Syrphi- the larva developed, so that the prepupae and pupae dae: 39%) (Hone ˇ k & Kocourek 1990 ). It may, however, are exposed to cannibalism or intraguild preda- exceed 40% in Axinoscymnus cardilobus (Huang et al. tion. The prevalence of parasitization of ladybird 2008 ) feeding on whitefl ies. The development rate of pupae by Phalacrotophora fl ies increases strongly with pupae is linearly and positively related to tempera- the population density of the pupae, reaching up to ture ( 3.6 ), and is usually independent on the prey 40% (Durska et al. 2003 ). Larvae of the genus Chilo- quality and quantity in the preceding larval stage corus aggregate before pupation (Fomenko 1970 , (Ahmad et al. 2006 ); by contrast, pupal and adult Fomenko & Zaslavskii 1970 ). weight are dependent on previous feeding. Pupae of In aphidophagous ladybirds, the place for pupa- Col. maculata from larvae fed with pollen reached tion is mainly foliage, while some coccidophagous 14 mg and lasted 3.2 days while those fed on artifi cial species pupate on the bark of branches and on tree diet weighed less (11 mg) and lasted for a comparable trunks. Cryptically coloured pupae tend to be hidden time (3.4 days) (Lundgren & Wiedenmann 2002 ). The on the underside surface of the leaves, while apose- complete pre- imaginal development of Hip. convergens matically coloured ones may be exposed on the upper on Thrips tabaci lasted 30 days, and 24 days on side and take advantage of basking in the sun (see Acyrthosiphon pisum, while the duration of the pupal thermal melanism, 3.4.6 ). stage was not affected by the food (Schade & Sengonca In central Honshu, hibernating and reproductive 1998 ). adults of C. septempunctata coexist in the same habitat
Under conditions of artifi cially elevated CO 2 con- during the mild winter. Although natural substrates centration , the pupal development time was affected; were available, the beetles preferred to use artifi - both the larval and pupal durations of Har. axyridis fed cial substrates such as metal cans (iron or alumin- Aphis gossypii were signifi cantly shorter than at the ium), papers, and wooden materials discarded on normal concentration (Chen et al. 2005 ). A high level the sunny slope as oviposition and pupation sites. of crowding (35 larvae per beaker) shortened subse- They were warmed by solar radiation and served as quent pupal development in P. dissecta (2.2 days in thermal microhabitats (Ohashi et al. 2005 ). About comparison to 3.4 days at low densities) (Omkar & 90% of the larvae of Col. maculata left the potato plant Pathak 2009 ). to pupate. They selected shelters that effectively A relatively high incidence of pupation was observed reduced their intraguild predation by the lacewing during the late photophase (09:00 – 12:00 hours, Chrysoperla rufi labris (Lucas et al. 2000 ). The larvae 76 O. Nedveˇ d and A. Honeˇk and pupae of the ladybird Thalassa saginata develop 3.4.6 Colouration and thermal melanism inside colonies of the ant Dolichoderus bidens (Orivel et al. 2004 ). Many coccinellid pupae are cryptically coloured , while in some large Coccinellinae the colours are bright and probably have a warning function. Species 3.4.5 Pupal defence such as C. septempunctata and Har. axyridis , which mostly pupate exposed on the upper leaf surface, Pupae covered by the larval skin are protected combine a bright orange background with black spots. mechanically, especially when the larva is spiny (Chi- The extent of melanization and the darkness of the locorinae, Epilachninae) or covered by waxy exuda- orange - brown background increases in both species tions (Scymninae). The pupal cuticle also has its own with decreasing temperature and increasing humid- hairs , which are especially long in the Epilachninae ity. The pupa is light orange at 35 ° C and dark brown and Scymninae, and often have a glandular function, at 15° C in C. septempunctata (Hodek 1958 , Okuda et al. containing defensive compounds. Transparent viscous 1997 ). In C. septempunctata, the percentage of the area droplets are visible on the tips of the setae of the pupa from dorsal and lateral views which is black decreases of Scymnus sinuanodulus (Lu et al. 2002 ). The white linearly (from 45– 55% to almost zero) with increasing pupa of Clitostethus oculatus has tiny clear droplets on temperature (from 20 to 36 ° C) (Rozsypalova 2007 ). the tips of the setae at high relative humidity. Larval Unlike the larvae and adults, which can control their exuviae together with whitefl y debris cover the tip of body temperature behaviourally, the pupa relies on the pupal abdomen. The yellowish pupae of Delphastus heating by the sun. pusillus are covered by short hairs without any secre- The sensitive stage for the determination of the tion, and several abdominal segments are enclosed extent of melanization is the late prepupa. Elements of within an unfragmented larval skin (Liu & Stansly the future elytral pattern may be visible on the pupal 1996a ). wingpads . In Har. axyridis , there is a similar trend as The surface of the pupa of the phytophagous Subcoc- in C. septempunctata, but shifted to lower temperatures cinella vigintiquatuorpunctata bears glandular hairs pro- (17 to 33 ° C) (Ungerov á & Nedv eˇ d, unpublished). The ducing three polyazamacrolide alkaloids. The secretion extent of melanization of the adult is independent of serves as a potent anti - predator defence against the the melanization of the pupa. predatory ant Crematogaster lineolata (Smedley et al. Blackening of the pupal case may also be caused by 2002 ). Comparative studies of the defensive chemistry infection, injury or intoxication. This was observed in of eggs, larvae, pupae and adults showed both qualita- pupae of C. septempunctata whose larvae had been tive and quantitative differences in alkaloid composi- treated with azadirachtin (Banken & Stark 1997 ). tion between the life stages of Epilachna paenulata Although the colouration of ladybird pupae is less (Camarano et al. 2006 ). The polyazamacrolide epil- variable and less striking than that of adults, pupae achnene, the principal component of the secretion of can still be identifi ed to species. For example, the the pupal defensive hairs of Epilachna varivestis , proved colour and spotting of prepupae and pupae provide to be a deterrent for Har. axyridis (Rossini et al. 2000 ). identifi cation characters to distinguish two sympatric The oily droplets on the pupal integumental hairs of ladybirds, Henosepilachna pusillanima and H. boisduvali the squash beetle Epilachna borealis contain a mixture that have indistinguishable adult colouration (Nakano of tocopheryl acetates (Attygalle et al. 1996 ) and & Katakura 1999 ). polyazamacrolides (Schroder et al. 1998 ). (more on semiochemicals in Chapter 9 ). The pupa is not entirely immobile. If irritated by a 3.5 ADULT predator or parasitoid, it quickly raises itself upwards several times. Pupae are better protected against preda- 3.5.1 Teneral development tion than prepupae, but in most species they are still susceptible to attack. The tough pupal integument Teneral development may include sexual maturation affords better protection than the soft larval skin (Ware and the acquisition of fl ight ability . In many coccinel- & Majerus 2008 ). lids, the activity of the follicular tissue in the testes Life history and development 77 starts in the pupa (Hodek & Landa 1971 , Hodek 1996 ). fl ightless beetles have a longer residence time on the After emerging from the pupa, females, and sometimes plants, even at lower prey density (Lommen et al. also males, show a refractory period of a few days in 2008 ). A homozygous fl ightless (but fully winged) their mating behaviour. This was found to be equal in strain of Har. axyridis was obtained by laboratory selec- males and females of A. bipunctata (Hemptinne et al. tion and used in biological control (Tourniaire et al. 2001 ). Slight protogyny (the fi rst mating of females 2000 ). This strain had not only a longer residence taking place at earlier age) could theoretically occur time on aphid- infested plants but also a minimal when females mate before sexual maturity and store potential to become invasive. Artifi cially, fl ightless sperm, while males mate only after maturity. Mating of ladybirds may be induced in a culture by limiting space sexually non- mature females is common in many during the emergence of adults from pupae individu- species with reproductive diapause (Chapter 6 ). Long ally placed into small chambers; this results in defor- refractory periods were observed in Sasajiscymnus mation of elytra and wings (N. Osawa, personal tsugae : at 25 ° C when males matured at 19 days, communication). whereas the female pre- oviposition period was 22.4 days (Cheah & McClure 1998 ). Omkar & Srivastava (2002) report protandry in Indian C. septempunctata . 3.5.3 Pre-oviposition period Males were ready to mate within 9 days at 27 ° C, while females took 11 days. Rana & Kakker (2000) reported The number of days between female emergence and an average pre- mating period in C. septempunctata of the laying of the fi rst egg batch is called the pre - 6.4 days. oviposition period. Its duration can be used to measure Temperature requirements for completing the the intensity of diapause (Chapter 6 ). In dormant teneral period may be calculated as for immature females, it can last weeks or even months. development ( 3.6 ) and may be prolonged by unsuitable Interspecifi c variation in the pre - oviposition prey (Hukushima & Kamei 1970 ) or prey scarcity period can be substantial. In Coccinellinae, it ranges (Kawauchi 1981 ). between 0 and 10 days: in Har. axyridis it was 6 – 10 The basic sex ratio in coccinellids is close to 50:50, days, in A. bipunctata 3– 8 days and in Hip. variegata it except where there is an infection by a male- killing was surprisingly reported to be only 0– 4 days (Lanzoni agent (Chapter 8 ). An increased proportion of males et al. 2004 ), which would indicate that some females was found at high temperatures: in Har. axyridis at of this species completed the development of their eggs 30° C (62– 82%) (Lombaert et al. 2008 ) and in P. dis- while in the pupal stage. A short pre- oviposition secta at 35 ° C (62%) (Omkar & Pervez 2004b ). period of 2– 3 days was also found in Anegleis cardoni (Omkar et al. 2009 ). Adults of C. septempunctata fed on Sitobion avenae started mating 4 – 11 days after emer- 3.5.2 Wings and fl ight gence, with an average pre - mating period of 6.4 days (Rana & Kakker 2000 ). The ability to take- off matures within a short period In Scymninae , the pre - oviposition period varies after the moult to adult. Adults of C. septempunctata even among closely related species. In Scymnus frontalis began attempts to fl y 40 hours after emergence at 26° C it was 10 – 11 days (Gibson et al. 1992 ), while it was (Hon eˇ k 1990 ). Confi nement of ladybirds in a limited only two days in S. louisianae (Brown et al. 2003 ). In space increased both the willingness to take- off and contrast, long pre- oviposition periods of 13 days at the duration of fl ight in C. septempunctata (Nedve ˇ d & 31° C and 23 days at 20° C were observed in Clitostethus Hodek 1995 ). oculatus (Ren et al. 2002 ), and of 22 days at 25° C in There have been a few reports of the occasional Sasajiscymnus tsugae (Cheah & McClure 1998 ). occurrence of wingless or brachypterous individuals The pre - oviposition period generally increases at among normally winged ladybirds. Winglessness in A. lower temperatures : it ranged from 20.5 days at a bipunctata is determined by a single locus with the mean temperature of 15° C to 7.7 days at 30° C in wingless allele recessive to the winged wildtype allele Scymnus frontalis (Naranjo et al. 1990 ), from 9 days (Lommen et al. 2005 ) (Chapter 2 ). The occurrence of at 20° to 4 days at 35° C in S. levaillanti (Uygun & fl ightless ladybirds might increase biocontrol because Atlı han 2000 ) and from 24 days at 15° C and 3.5 days 78 O. Nedveˇ d and A. Honeˇk at 35 ° C in S. marinus (M ’ Hamed & Chemseddine 2001 ). abundant. Large ladybirds cannot be sustained by low Food suitability also modifi es the pre- oviposition densities of small aphids due to the food limitation period: this was shorter in Menochilus sexmaculatus fed (Sloggett 2008 ). with Aphis craccivora , Aulacorthum solani , Sitobion akebiae, and Myzus persicae (7.3– 8.0 days) than when fed with A. gossypii (11.6 days) (Sugiura & Takada 3.5.5 Ovarioles 1998 ). The ovarioles of Coccinellidae are of the meroistic telotrophic type. The number of ovarioles is species - 3.5.4 Size specifi c, as well as dependent on the conditions during the larval development of the female (Table 3.2 ). There Females are generally larger and heavier than males, is a higher number of ovarioles in larger species; the although often not signifi cantly so, due to high varia- number increases with body length by the power func- bility. The fresh weight of emerged females of Anegleis tion with the exponent of 1.14 ± 0.02 (Fig. 3.6 ). cardoni was constantly 1.16- times higher than that of Species with few ovarioles lay larger eggs than similar- males when reared on three different prey species, sized species with many ovarioles (Stewart et al. 1991b ; while the difference in weight within each of the 5.2.3). The number of ovarioles has been reviewed two sexes between being fed the most and the least from the viewpoint of taxonomy, evolution and fecun- suitable prey species was 1.35 times (Omkar et al. dity by Rathour and Singh (1991) . In species with a 2009 ). Newly emerged females of Har. axyridis were high number of ovarioles, there is a smaller number 1.1 to 1.2- times heavier than males (Ungerová et al. of chambers (follicles) with ripening oocytes (three in 2010 ). C. septempunctata) than in species with a small number The positive relationship between male and female of ovarioles (eight in Stethorus sp.) (Dobrzhansky weight under the same conditions is linear after log– 1926 ). log transformation, giving the equation log W M = Intraspecifi c comparisons in C. septempunctata
– 0.07 + 0.97 log WF . for A. bipunctata and WM = showed a positive linear relationship between the
– 0.043 + 0.96 log WF . for P. japonica (Dixon 2000 ). number of ovarioles and female body weight (Dixon Crowding of larvae in a small space reduced adult size & Guo 1993 ). The mean number of ovarioles in C. of P. dissecta: 7 mg with single individuals, 11 mg at 4 septempunctata females of 24 mg body weight was 80, individuals per beaker (0.7 l), and only 5 mg at 35 per while it was 139 in females weighing 31 mg (Rham- beaker (Omkar & Pathak 2009 ). In small (7 cm) Petri halinghan 1985, 1986 ). In contrast, no correlation of dishes, the mean mass of Har. axyridis was 18.8 mg; in the number of ovarioles with either body length or 15 cm Petri dishes 21.2 mg; in 0.5 l jars 25.1 mg body weight of females was found in Har. axyridis (Ungerov á et al. 2010 ). (Nalepa et al. 1996 , Osawa 2005 ). Body length and width decreased as constant tem- Effects on the reproductive output of the resulting peratures increased from 22 to 34 ° C in Chil. nigritus , females of the diet provided to larvae have been but were highest at an alternating temperatures reported. The number of ovarioles was 10% lower in regime of 20/34 ° C (Ponsonby 2009 ). Females were A. bipunctata fed on the suboptimal prey Aphis cracciv- only 1.03- times longer than males. ora than in females fed with the high quality prey Apart from using body length and weight, the Acyrthosiphon pisum (Ferrer et al. 2008 ). However, ventral body area (mm 2) may be calculated by measur- Ware et al. (2008b) reported no effect of larval diet on ing the body length and width and using the formula ovariole number in Har. axyridis and A. bipunctata , [ ½ (body length)] × [ ½ (body width)] (Obrycki et al. although maximum clutch size and oviposition rate 1998 , Giles et al. 2002 , Phoofolo et al. 2007 ). were affected. Starvation does not alter the total In interspecifi c comparisons among aphidophagous number of ovarioles, it only changes the percentage of ladybirds, body size of a species is related to the body oosorptive and mature ovarioles (Osawa 2005 ). In size and density of the prey. Small ladybirds can feed those individuals of C. septempunctata with less than on small aphid species when these are in both high and 100 ovarioles per female, almost all of the ovarioles low densities, but on large aphid species only at high (99.8%) were healthy and functional. By contrast, densities, where young instars of the aphids are in individuals with a high ovariole number (102 to Life history and development 79
Table 3.2 Number of ovarioles per ladybird female, female weight (mg) and size (mm). Indicated are ranges or mean numbers of ovarioles in both ovaries together, if directly referred to in the literature source in the right column, or double the number of ovarioles per one ovary if given so in the source. Size and fresh weight of each species are either original unpublished data measured by N edv e ˇd, or measured by R hamhalinghan (four rows marked by asterisk * ); averaged literature data on body length are given for other species. See also Fig. 3.6 . Species Weight Size Ovarioles Reference Adalia bipunctata — — 45–51 Dobrzhansky (1926) Adalia bipunctata — — 47 Ferrer et al. (2008) Adalia bipunctata 13.5 4.9 43 Ferrer et al. (2008) Adalia bipunctata — — 48 Ware et al. (2008) Adalia decempunctata 10.7 4.6 48–52 Dobrzhansky (1926) Adalia tetraspilota — 4.5 34–48 Rathour & Singh (1991) Afi denta misera — 5.4 40–48 Rathour & Singh (1991) Afi ssula rana — — 26 Rathour & Singh (1991) Afi ssula sanscrita — — 18 Rathour & Singh (1991) Aiolocaria hexaspilota — 9.7 91 Dobrzhansky (1926) Aiolocaria hexaspilota — 9.7 88–96 Rathour & Singh (1991) Alloneda dodecaspilota — 6.8 32–44 Rathour & Singh (1991) Anatis ocellata 60.7 8.5 56 Dobrzhansky (1926) Anegleis cardoni — 3.7 20 Rathour & Singh (1991) Anisosticta novemdecimpunctata — 3.5 24 Dobrzhansky (1926) Apolinus lividigaster — 4.0 14–26 Anderson (1981) Callicaria superba — 11.5 52–60 Rathour & Singh (1991) Calvia albida — 8.0 18–24 Rathour & Singh (1991) Calvia decemguttata 27.3 6.6 29 Dobrzhansky (1926) Calvia quatuordecimguttata 22.7 5.4 40 Dobrzhansky (1926) Calvia quatuordecimguttata 22.7 5.4 40 Semyanov (1980) Calvia shiva — — 28–36 Rathour & Singh (1991) Calvia shiva pasupati — — 22 Rathour & Singh (1991) Calvia shiva pinaki — — 18 Rathour & Singh (1991) Calvia shiva trilochana — 4.9 22 Rathour & Singh (1991) Calvia sp. — — 24–28 Rathour & Singh (1991) Ceratomegilla undecimnotata 44.0 6.6 42–62 Dobrzhansky (1926) Chilocorus bijugus — — 40–48 Rathour & Singh (1991) Chilocorus bipustulatus — 3.5 25 Dobrzhansky (1926) Chilocorus breiti — — 18–24 Rathour & Singh (1991) Chilocorus hauseri — — 30–40 Rathour & Singh (1991) Chilocorus nigritus — 4.0 18 Rathour & Singh (1991) Chilocorus rubidus — 6.5 72–80 Rathour & Singh (1991) Chilocorus sp. — — 32–40 Rathour & Singh (1991) Chilocorus sp. — — 24–32 Rathour & Singh (1991) Coccinella hieroglyphica — 3.5 34 Dobrzhansky (1924) Coccinella hieroglyphica — — 28 Dobrzhansky (1926) Coccinella luteopicta — 5.8 44–52 Rathour & Singh (1991) Coccinella magnifi ca — 7.4 69–74 Dobrzhansky (1926) Coccinella septempunctata — — 96–119 Dobrzhansky (1926) Coccinella septempunctata 44.4 7.2 102 Klausnitzer & Klausnitzer (1986) Coccinella septempunctata — — 108–124 Rathour & Singh (1991) Coccinella septempunctata 30.5* — 129 (57 –82 pairs) Rhamhalinghan (1985) Coccinella septempunctata 23.6* — 86 (26 –61 pairs) Rhamhalinghan (1985) Coccinella septempunctata 31.6* — 149 Rhamhalinghan (1986) Coccinella septempunctata 24.2* — 74 Rhamhalinghan (1986) (Continued) 80 O. Nedveˇ d and A. Honeˇk
Table 3.2 (Continued) Species Weight Size Ovarioles Reference Coccinella undecimpunctata — 5.0 68 Dobrzhansky (1926) Coccinula quatuordecimpustulata — 3.5 20 Dobrzhansky (1926) Coccinula redimita — 4.0 20 Dobrzhansky (1926) Coelophora bissellata — 5.3 26–36 Rathour & Singh (1991) Coelophora duvaucelii — — 36–44 Rathour & Singh (1991) Cryptogonus ariasi — 2.2 14 Rathour & Singh (1991) Cryptogonus orbiculus — — 14 Rathour & Singh (1991) Cryptogonus postmedialis — — 14 Rathour & Singh (1991) Cryptogonus quadriguttatus — — 14 Rathour & Singh (1991) Epilachna dumerili — — 24–32 Rathour & Singh (1991) Epilachna marginicollis — — 32–36 Rathour & Singh (1991) Epilachna mystica — — 44–52 Rathour & Singh (1991) Exochomus quadripustulatus 9.7 4.3 26 Dobrzhansky (1926) Halyzia sanscrita — — 38–44 Rathour & Singh (1991) Halyzia straminea — 7.3 56–64 Rathour & Singh (1991) Harmonia axyridis — — 54–78 Dobrzhansky (1924) Harmonia axyridis 34.7 6.5 64–76 Dobrzhansky (1926) Harmonia axyridis — — 53–77 Fois & Nedve ˇ d, unpubl. Harmonia axyridis — — 62 (44 –84) Nalepa et al. (1996) Harmonia axyridis — — 62 Ware et al. (2008) Harmonia dimidiata — 8.3 50–60 Rathour & Singh (1991) Harmonia eucharis — 8.0 48–164 Rathour & Singh (1991) Harmonia quadripunctata 22.3 6.1 36–40 Dobrzhansky (1926) Harmonia sedecimnotata — 6.5 54–64 Rathour & Singh (1991) Henosepilachna dodecastigma — — 56–60 Rathour & Singh (1991) Henosepilachna indica — — 44–54 Rathour & Singh (1991) Henosepilachna ocellata — — 58–64 Rathour & Singh (1991) Henosepilachna processa — 9.1 54–58 Rathour & Singh (1991) Henosepilachna pusillanima — 8.1 63 Dobrzhansky (1926) Henosepilachna sp. — — 34 Rathour & Singh (1991) Henosepilachna vigintioctomaculata — — 55 Dobrzhansky (1926) Henosepilachna vigintioctomaculata — 7.4 48–56 Rathour & Singh (1991) Henosepilachna vigintioctopunctata — 6.4 56–72 Rathour & Singh (1991) Henosepilachna vigintioctopunctata — — 84 Dobrzhansky (1926) Hippodamia septemmaculata — 6.0 40–46 Dobrzhansky (1926) Hippodamia tredecimpunctata — 5.9 48–60 Dobrzhansky (1926) Hippodamia variegata 10.3 4.8 45–49 Dobrzhansky (1926) Hippodamia variegata — — 42–48 Rathour & Singh (1991) Hyperaspis campestris 4.7 2.9 19–21 Dobrzhansky (1926) Hyperaspis reppensis — 2.8 17–20 Dobrzhansky (1926) Illeis cincta — 4.0 38–44 Rathour & Singh (1991) Jauravia quadrinotata — 2.2 18 Rathour & Singh (1991) Megalocaria dilatata — 13.0 40–52 Rathour & Singh (1991) Menochilus sexmaculatus — 5.0 40–52 Rathour & Singh (1991) Micraspis allardi — 4.5 28 Rathour & Singh (1991) Myrrha octodecimguttata 11.3 4.3 16–17 Dobrzhansky (1926) Myzia oblongoguttata 39.0 7.5 41–46 Dobrzhansky (1926) Nephus redtenbacheri — 1.6 12 Dobrzhansky (1926) Oenopia billieti — 3.9 24 Rathour & Singh (1991) Oenopia conglobata — — 24 Dobrzhansky (1926) Oenopia conglobata 11.0 4.6 24 Nedveˇ d, unpubl. Oenopia kirbyi — 3.3 24 Rathour & Singh (1991) Life history and development 81
Table 3.2 (Continued) Species Weight Size Ovarioles Reference Oenopia sexareata — — 24 Rathour & Singh (1991) Palaeoneda auriculata — 10.5 84–88 Rathour & Singh (1991) Pania luteopustulata — 5.1 24–32 Rathour & Singh (1991) Platynaspis luteorubra — 3.0 19–22 Dobrzhansky (1926) Priscibrumus uropygialis — — 24 Rathour & Singh (1991) Propylea quatuordecimpunctata 13.0 4.1 23 Dobrzhansky (1926) Psyllobora vigintiduopunctata 7.7 3.8 22–24 Dobrzhansky (1926) Lindorus lophanthae — 2.5 20 Stathas et al. 2002) Rodolia guerini — — 40 Rathour & Singh (1991) Rodolia sp. — — 24 Rathour & Singh (1991) Scymnus ater — 1.5 8 Dobrzhansky (1926) Scymnus frontalis 3.1 2.5 12 Dobrzhansky (1926) Scymnus haemorrhoidalis 1.3 2.1 10–12 Dobrzhansky (1926) Scymnus interruptus — 2.2 12 Dobrzhansky (1926) Scymnus nigrinus 3.0 2.6 12 Dobrzhansky (1926) Scymnus rubromaculatus 1.9 2.2 10–12 Dobrzhansky (1926) Scymnus suturalis 0.9 1.8 14 Dobrzhansky (1926) Stethorus pusillus 0.6 1.4 4 Dobrzhansky (1926) Subcoccinella vigintiquatuorpunctata 13.3 3.8 33–35 Dobrzhansky (1926) Tytthaspis sedecimpunctata 5.3 3.0 20–21 Dobrzhansky (1926) Vibidia duodecimguttata — 4.0 24 Dobrzhansky (1926)
180
160
140
120
100
80
60
40
20 Body mass [mg]; Ovariole number Ovariole [mg]; Body mass
0 02468101214 Body length [mm]
Figure 3.6 Relationships between body length (mm), body mass (mg, diamonds) and number of ovarioles (open circles) in Coccinellidae. Sources of the numbers of ovarioles are listed in Table 3.2 . Fresh body masses are data measured by Nedve ˇ d (unpublished), body length are either measured by Nedve ˇd or averaged literature data. Body mass increases with body length with the power function M = 0.27 · L 2.46, number of ovarioles follow the power function (close to linear) NO = 6 · L1.14 . 82 O. Nedveˇ d and A. Honeˇk
200 ovarioles per female), approximately 5.6% of the The mating duration was recorded as 54 minutes ovarioles were dysfunctional. The effi ciency of the with a range of 41– 62 minutes in C. septempunctata ovarioles (percentage of simultaneously active ones) (Rana & Kakker 2000 ). The duration was higher (51 was high in the summer generation and low in the minutes) when a melanic female mated with a melanic winter generation. Crowding and competition among male of Indian C. septempunctata and lower (39 the ovarioles and inadequate nutrition were the minutes) when a typical female mated with a typical factors affecting ovarian dysfunction (Rhamhalinghan male (Srivastava & Omkar 2005 ). Typical duration of 1986 ). mating of Har. axyridis in laboratory was between 2 A fi ve- stage rating system to describe ovarian devel- and 3 hours (Awad & Nedv eˇ d, unpublished). The opment is based on the length of the terminal follicle , mating posture in Aiolocaria hexaspilota may last several the number and shape of developing follicles in each days (Iwata 1932 ). Manipulating the mating duration ovariole, and the presence of yellow colour (yolk ) artifi cially had a dramatic infl uence on hatching rate in the terminal oocyte (Okuda et al. 1986 , Phoofolo in Menochilus sexmaculatus and Coelophora saucia et al. 1995 ). Fully developed oocytes are vitellinized (Omkar et al. 2006a ). No eggs were fertilized after (yolk is deposited) and chorionated (covered by a copulation lasting only 10 seconds, about 35% of eggs chitinous envelope). A positive linear relationship has after a 1 minute copulation, and 80 – 90% after copula- been observed between ovarian developmental rate tion lasting 1 hour or a natural long copulation. and temperature. Oocytes gradually grow and ripen in Mating rhythmicity . Mating in Menochilus sex- individual ovarioles, and may then be laid synchro- maculatus (Omkar & Singh 2007 ) and P. dissecta nously from one or both ovaries. The number of eggs (Mishra & Omkar 2004 ) in India occurred at all times laid is positively correlated with the number of ovari- of the day or night with a slight prevalence (66%) oles, body length and body weight. during the photophase . The rates of ovarian development and oosorption The willingness to mate of both males and females in predatory Har. axyridis are much higher than in her- of P. dissecta increased until their age had reached bivorous ladybirds. During starvation , the nutrients 10– 30 days (Pervez et al. 2004 ). In C. septempunctata were found to be resorbed back from developing eggs. in India, females started to mate at 2 days and males This oosorption mainly occurred during the intermedi- at 4 days after emergence. Ten day old males and ate developmental stage of the ovarioles, and the females were the most willing to mate (Srivastava & ovarian development and oosorption were asymmetric Omkar 2004 ). Mating of young (1– 5 day old) adult in the right and left ovaries in Har. axyridis (Osawa P. dissecta lasted about 200 minutes; mating of those 2005 ). 20 days old lasted about 300 minutes (Pervez et al. 2004 ). The willingness to mate strongly increases when adults have no chance to mate. Col. maculata 3.5.6 Mating where the genders were isolated for only 1 day were 26 times more likely to mate than individuals kept in a 3.5.6.1 Frequency and d uration of m ating mixed- sex group; isolating males had a stronger effect than isolating females (Harmon et al. 2008 ). Ladybirds mate often and for a long time, and change Multiple matings usually enhance the total egg partners (i.e. they are promiscuous ). A mating fre- output and percentage of eggs that hatch, even though quency of about 20% at any given time was recorded one copulation is suffi cient for permanent fertility of for A. bipunctata in the fi eld (Haddrill et al. 2007 ). The the female (except in some species such as Stethorus male uses his legs to hold himself onto the elytra of the pusillus that lack a spermatheca; Putman 1955 ). female and is carried by her. Body shaking by males Mating had a repeated stimulatory effect on the is essential for insemination. The spermatophore is number of eggs laid in A. bipunctata (Semyanov 1970 ). formed in the bursa copulatrix (Obata 1988 ). Within The hatching rate in Menochilus sexmaculatus was 64% 1 hour of mating the spermatophore is emptied, the after multiple matings and 37% after only a single envelope ejected from female’ s reproductive organs mating (Bind 2007 ). Egg hatching rate in this species and is usually eaten by the female (Obata & Hidaka decreased after separation of the female and male: 1987 ). hatching was reduced to 50% by 50, 40 and 30 days Life history and development 83 after the separation (following 5, 10 and 20 matings, females of P. dissecta were also more fecund and laid respectively) (Omkar & Mishra 2005a ). Results with more viable eggs than monogamous ones, which had P. dissecta (Omkar & Pervez 2005 ) were even more been confi ned in a cage with a single male. Amongst striking: 65% eggs hatched after a single mating, 72% promiscuous females, those mated with several males after two, 78% after three and 93% after further mul- (i.e. there was freedom of mate choice) had a signifi - tiple mating. However, the physical interference cantly higher reproductive output than those mated between individuals in a limited space had a small daily with a new unmated male with no choice (Omkar detrimental effect on egg viability of P. dissecta : 96% & Mishra 2005a ). of the eggs laid by a single mated female hatched, while only 88% of the eggs hatched when laid by a female sharing a 9 cm Petri dish with four unmated males 3.5.6.2 Sperm c ompetition (Mishra & Omkar 2006 ). Earlier studies suggested that most often it was the Mating (or repeated mating) refusal by ladybird sperm of the last male (of many that copulated with females has been observed frequently, but the causes the female) that fertilized the eggs (Ueno 1994, 1996). and consequences of such behaviour have rarely been De Jong et al. (1993) provided evidence for almost revealed. Two prominent hypotheses are that resist- complete second male sperm precedence in experi- ance is (i) a means of avoiding costly and dangerous ments with melanic and non- melanic A. bipunctata mating and (ii) a means for the selection of high- providing that the results were not obscured by female quality males. Female refusal may be decreased by a rejection behaviour . In a repeated experiment, nutritious nuptial gift, i.e. a spermatophore, provided however, there was a highly variable degree of pater- by the male. The above hypotheses were investigated in nity of the second male (de Jong et al. 1998 ). A. bipunctata , in which females frequently display Behavioural and molecular genetic data were used strong copulation rejection behaviour and ingest to examine how sperm from several males was used a spermatophore after copulation (Perry et al. over time by females of A. bipunctata , and to link mating 2009 ). Females deprived of food for 96 hours resisted with fertilization (Haddrill et al. 2008 ). In the labora- mating more frequently and for longer periods than tory, the number of mates (males that copulated with less starved females (starved for only 16 hours) and so the observed female) was usually similar to the number they re- mated less frequently. The fi nding that starved of fathers (males that passed their genes to the females were more resistant suggests that mating is progeny), suggesting that females have little post- energetically costly, and that nuptial consumption of copulatory infl uence on the paternity of their eggs. spermatophores does not offset these costs (Perry et al. Longer copulation resulted in a higher probability of 2009 ). paternity for any particular male, probably due to the Female longevity decreased with increasing number transfer of larger numbers of sperm in multiple sper- of matings in both Menochilus sexmaculatus and P. dis- matophores (Haddrill et al. 2008 ). secta, indicating there is a cost to mating. Thus very high mating activity, typical of many ladybirds, may have a deleterious effect on their fi tness (Omkar & 3.5.6.3 Female c hoice and m elanism Mishra 2005a ). Longevity decreased from 118 days for single, once - mated females to 76 days for repeatedly Hodek and Ceryngier (2000 ) regarded the fi nding that mated females of Har. axyridis. Due to this difference, at least some coccinellid species do not mate at random once - mated females had higher lifetime fecundity as the most important among the sexual activities of (1326 eggs, hatchability 58%) than repeatedly mated coccinellids. ones (977 eggs, 51%; Fois et al. unpublished). To fi nd out whether ladybird females prefer a specifi c There was a transient benefi t from polyandry male phenotype, e.g. a colour morph in polymorphic (mating with several different males) in the reproduc- species, choice and no - choice mating tests can be tive success of A. bipunctata females. Fecundity and conducted. Also, observations can be made of sea- hatching rate were lower in females mated 10 times sonal changes in the frequency of colour morphs with one male than in females mated once with 10 (individuals) and of pairs of different composition in different males (Haddrill et al. 2007 ). Promiscuous the fi eld. 84 O. Nedveˇ d and A. Honeˇk
Lusis (1961) observed that matings of A. bipunctata may vary between generations: (i) maternal factors recorded near Riga and Moscow involved fewer matings (epigenetic) that infl uence the expression of genes in between red females and red males and signifi cantly progeny, and (ii) linkage disequilibria among allele more black males in pairs than would be expected with frequency that cycle seasonally as a function of random mating. He hypothesized that the higher assortative mating (Wang et al. 2009 ). sexual activity of the melanic forms was due to their In fi eld populations of Har. axyridis in China, red higher metabolic rate, as the result of higher absorb- phenotypes outnumbered melanics by 5:1 in the ance of solar radiation. However, Creed (1975) did not autumn, but melanics became equally abundant in the observe this phenomenon in a population of A. bipunc- spring, suggesting that melanism is advantageous in tata near Birmingham. Also in England, Muggleton winter, but costly in summer (Wang et al. 2009 ). In A. (1979) found that mating preference was affected by bipunctata, melanic forms were more abundant in the the frequency of the different forms: regardless of autumn than in the spring but not signifi cantly so colour, the rarer morph was preferred by females of (Majerus & Zakcharov 2000 , Hon eˇk et al. 2005 ). The both morphs. Majerus et al. (1982a) reported a prefer- representation of melanic males in mating pairs ence for melanic males in another English population observed in a cage experiment was higher than would in 1981: while 34% of the non - mating males of A. be expected from random mating (Majerus et al. 1982a). bipunctata in North Staffordshire were melanics, the Though it is still unknown how females recognise melanic proportion of mating males was 49%. For melanic males, as pointed out above, O ’ Donald and melanic females, however, the proportion was about Majerus (1989) were able to show that visual dis- 35% for both mating and non - mating ones. The crimination by females was not involved. Specifi c authors (Majerus et al. 1982b ) demonstrated a genetic cuticular alkanes (Hemptinne et al. 1998 ) may be basis for such preferential mating; differential competi- responsible for the recognition, and higher body tem- tiveness among males was not involved. However, the perature and activity in melanic A. bipunctata under mechanism whereby females recognize melanic males most conditions has been recorded (De Jong et al. 1996 ). remains unknown. In the related A. decempunctata , the proportion of the Female Har. axyridis expressed visible mate prefer- three main colour morphs ( typica , spotted; decempustu- ence, by rejecting less- preferred phenotypes, and cryp- lata , chequered; bimaculata , melanic) was found to be tically by retaining eggs for longer periods after very stable both in space and time, with no environ- mating with less - preferred males, apparently in order mental selection or female choice (Banbura & Majerus to replace their sperm later by that of a more- preferred in Majerus 1998 , Hon eˇk et al. 2005 ). male. Whereas pair formation was under female Females of Har. axyridis uninfected with the ectopar- control, the duration of copulation was under male asitic fungus Hesperomyces virescens were preferred by control. Males invested more time in mating with dis- males as mating partners over infected ones (Nalepa similar females (Wang et al. 2009 ). Which males were & Weir 2007 ). preferred was not clear- cut, because there was a pleio- Melanic as well as typical individuals of C. septem- tropic effect whereby female choice varied between the punctata in India preferred to mate with melanic forms spring and autumn generations. The prevalence of of the opposite sex. Mate choice was mainly deter- melanics in spring decreased in summer because mined by females and to a lesser degree by males females preferred mating with the pale succinea morph (Srivastava & Omkar 2005 ). While Osawa (1994) sug- (Osawa & Nishida 1992 ). In the summer generation, gested that the colour of the elytra of Har. axyridis is melanics were more successful. the most important factor in mate choice by females, Several studies based on mate - choice experiments Ueno (1994) stressed that size and activity were have shown that most females seemed to prefer to mate important. with melanic morphs, especially the conspicua morph. Perry et al. (2009) investigated whether the extent Thus melanics dominate in laboratory cultures and of active choice/rejection of males by females depended biocontrol stocks although they remain relatively on male size or whether unspecifi ed rejection pas- rare in the wild due to a set of selection pressures (Seo sively favoured large males that overwhelmed the et al. 2008 ). females. They found that the extent of female resist- Two alternative hypotheses have been offered to ance was independent of the size of the male, but that explain why gender- specifi c reproductive behaviour limited resistance resulted in a bias towards large males Life history and development 85 in copulations. A side effect of imperfect female resist- requirements which may sometimes even be confl ict- ance would be expected to result in selection for large ing: optimum microclimate for embryonic develop- male size. However, in all ladybirds, males are still ment, proximity of food for the hatched larvae, and slightly smaller than females, as also applies for the protection from predators, parasites and competitors majority of animals, refl ecting the higher energetic ( 5.4.1.3 ). and nutritional cost of producing eggs in comparison The Coccidulini lay eggs freely on the leaf surface with sperm. (Klausnitzer & Klausnitzer 1986 ). Megalocaria dilatata (Coccinellini) lays eggs on the spines of plants and makes a barrier preventing an access to the egg cluster 3.5.6.4 Hybridization with a sticky secretion from the abdomen (Liu 1933 ). Cases of spontaneous interspecifi c mating in the The aphidophagous generalist A. bipunctata laid more wild are rarely reported but may occur relatively often eggs (91%) on fi lter paper than on spruce needles (9%; in a limited space in the laboratory. Cases of successful Timms & Leather 2007 ), while the conifer adelgid- interspecifi c reproduction, i.e. hybridization are even eating specialist Aphidecta obliterata laid more eggs on rarer. Majerus (1997) listed the observations of inter- needles (77%). Many aphidophagous coccinellids lay specifi c matings in the fi eld (fi ve combinations, includ- eggs on the underside of fi lter paper when in labora- ing taxonomically distant species) and laboratory tory containers, as in the fi eld they lay eggs on the (eight combinations, also with unrelated species). underside of the leaves on broad - leaved plants. In this There were either no progeny after such mating or the way the coccinellids may reduce the risk of predation progeny were apparently of the same species as the and rain washing off the eggs. Ladybirds specialised on female, suggesting that the female was already mated conifer trees lay eggs on the needles or into bark with the same species male. The only hybrid progeny crevices. were reported for a couple consisting of an A. bipunc- In Japan, C. septempunctata used for oviposition arti- tata female and an A. decempunctata male. In other fi cial insolated objects during the winter (Ohashi et al. hybridization combinations using previously isolated 2005 ). A. bipunctata avoided laying eggs in patches females, eggs showed signs of development but did not with Lasius niger ants (Oliver et al. 2008 ). hatch ( embryonic mortality), or larvae died in the Scymninae often hide their eggs in crevices of the fi rst instar (Anatis ocellata × An. labiculata). A hybrid substrate, or use an artifi cial protection. Females of between P. quatuordecimpunctata and P. japonica had Sasajiscymnus kurohimae, feeding on eusocial aphids, decreased fecundity (Iablokoff - Khnzorian 1982 ). which have a soldier caste that defend their colonies, Reproductive isolation between two related protect their eggs beneath undigested remnants of Henosepilachna species is achieved by a combination of eaten aphids (Arakaki 1988 ). Scymnus hoffmanni simi- two mechanisms: (i) there is a choice for conspecifi c larly covers its eggs with cuticles of predated aphids females by Henosepilachna vigintioctomaculata males; (ii) (Kawauchi 1985 ). Eggs of Scymnus louisianae are laid there is a difference in the intensity of male rejection predominately on the undersides of leaves, nestled between H. vigintioctomaculata females (strong) and H. among the leaf hairs (Brown et al. 2003 ). pustulosa females (weak) (Matsubayashi & Katakura Females of Chilocorinae (e.g. Chil. rubidus ) lay one 2007 ). Host fi delity functioned as a strong barrier egg at a time under the scale of a larval prey coccid against gene fl ow between two other species Henosepil- (Pantyukhov 1968 ). Exochomus fl avipes have occasion- achna niponica and Henosepilachna yasutomii, but occa- ally been observed laying eggs into a conspecifi c empty sional interspecifi c mating has been achieved by pupae from which a parasitoid had emerged (Geyer addition of common host plant (Hirai et al. 2006 ). 1947 ). Two whitefl y predators, Clitostethus oculatus (Scymn- inae) and Delphastus pusillus (Microweiseinae) lay eggs 3.5.7 Oviposition singly or in groups of 2 – 4 on leaf surfaces, where whitefl y eggs and nymphs are abundant (Liu & Stansly 3.5.7.1 Oviposition s ubstrate 1996a ). In Epilachninae that feed on plants as both adults Ovipositing females have to select a suitable place for and larvae, it is often diffi cult to distinguish oviposition their eggs. This selection involves balancing several preference from adult feeding preference, because 86 O. Nedveˇ d and A. Honeˇk oviposition is likely to occur at or near feeding sites. In second power curve (Omkar et al. 2009 ). The estima- laboratory assays, the distance between adult feeding tion of age at peak oviposition tends to be higher when scars and egg masses of Henosepilachna niponica was fi tted by this parabolic curve than when using an long (25 cm) and the females often placed eggs on arti- asymmetric distribution, and higher for treatments fi cial substrates rather than leaf discs (Fujiyama et al. giving long (usually in better conditions) than short 2008 ). oviposition periods (less suitable conditions). Omkar & Mishra (2005) distinguished between short - lived females, that distributed their reproduction uniformly 3.5.7.2 Oviposition r hythmicity in their lifetime, and long - lived females which showed a high burst of reproductive activity followed by a Many activities of ladybirds take place during the day, gradual decline. whereas they rest during the night ( 5.4.1.1 ). However, Egg production in Scymnus louisianae was found to the oviposition activity of several species in India decrease slowly, and it was rather equally distributed showed the opposite trend (Fig. 3.3 ). There, it was over a female lifespan of 80 days, though there was a found that C. septempunctata females preferred to ovi- rapid increase during 6 days after adult eclosion and a posit at the end of the scotophase and in the early rapid drop during last 10 days of life (Brown et al. photophase hours (21.00 – 1.00, where 0.00 means 2003 , Fig. 3.7 g). The females of Exochomus quadripus- the beginning of the photophase), P. dissecta laid 86% tulatus laid eggs in an irregular pattern, with the eggs during the early half of scotophase (Mishra & number of eggs deposited within a single day ranging Omkar 2004 ) or that they laid most eggs in the middle from 1 to 11 at a thermoperiod of 9/19 ° C and from 1 of the scotophase (15.00– 17.00). C. leonina transversa- to 16 eggs at 12/24 ° C; the oviposition rate had a rather lis laid most by dusk, i.e. at the beginning of the sco- bimodal appearance (Sengonca & Arnold 2003 ; Fig. tophase (11.00 – 13.00) (Omkar et al. 2004 ). In 3.7 h). The rate of egg production of Chil. nigritus fol- Menochilus sexmaculatus (Omkar & Singh 2007 ), the lowed a cyclical pattern that lasted for approximately peak of oviposition (62%) was attained during early 22 days (Ponsonby & Copland 2007 ). scotophase (12:00 – 15:00). The daily oviposition rates of C. septempunctata and P. quatuordecimpunctata were not related to female size 3.5.7.3 Oviposition r ate (Hon eˇk et al. 2008 ). Natality (m x), which is the mean number of female The number of eggs laid per day, i.e. daily oviposition offspring produced per surviving female during age or reproductive rate, increases rapidly during several interval x (Birch, 1948 ), is sometimes used instead of days after adult eclosion, to reach a maximum (which oviposition rate. The natality of Clitostethus oculatus may equate to the number of ovarioles in both ovaries fl uctuated many times during the lifespan of females of the female) at about two or three weeks, and then (Fig. 3.7 b), and did not follow the typical triangular slowly decreases during the remaining life span of the fecundity function referred to above (Ren et al. female, which might be several months. 2002 ). These changes in oviposition rate (rapid increase fol- lowed by slow decrease) during adult life can be 3.5.7.4 Oviposition p eriod described by a triangular fecundity function (Dixon 2000 ). The pattern can be fi tted by a third order power The duration of the period between the fi rst and the function (see fi g. 2.11b in Dixon 2000 ) or by the Bieri last egg batch, the oviposition period, is a good measure model (Bieri et al. 1983 , for its use see Lanzoni et al. of individual fi tness . The number of days between the 2004 , and Fig. 3.7 c). The Bieri model (Or = (a · (age − b))/ last oviposition and death of the female is called the (exp(c · (age − b)))) provides a calculation for the time of post- oviposition period. It can be zero, when a peak oviposition rate. The age specifi c oviposition female dies during its reproductive phase, or can rate can also be fi tted by a lognormal or other asym- last from a few days to weeks in senescent females. metric distribution curve. When a mean oviposition rate is calculated from the The increase and decrease of oviposition rate ( age total lifetime fecundity of a female, only the reproduc- specifi c fecundity) can also be almost symmetric, as tive (= oviposition) period should be used in the in Anegleis cardoni, where it was fi tted simply by a denominator. (a) 2.0 (b) 1.0
1.8 0.9
1.6 0.8
1.4 0.7
1.2 0.6
1.0 0.5
0.8 0.4
0.6 0.3 Natality [egg/day] Natality
0.4 0.2
0.2 0.1
0.0 0.0 04080120160 020406080100120
(c) 35 (d) 16
30 14
12 25 10 20 8 15 6 10 4 Oviposition rate[egg/day] 5 2
0 0 0 20406080100 0 10203040
(e) 14 (f) 50
45 12 40
10 35
30 8 25 6 20
4 15 10 Oviposition rate [egg/day] rate Oviposition 2 5
0 0 0 102030405060 0 20406080
(g) 3.0 (h) 12
2.5 10
2.0 8
1.5 6
1.0 4
Oviposition rate [egg/day] 0.5 2
0.0 0 020406080 0 10203040 Age [days] Age [days]
Figure 3.7 Age specifi c oviposition rates calling into question the general occurrence of the triangular fecundity function
(Dixon 2000 ). (a) Triangular natality (m x) with tail, Axinoscymnus cardilobus at 20° C fed with Bemisia tabaci (after Huang et al. 2008 ); (b) polymodal increasing natality of Nephaspis oculatus at 31° C fed with Bemisia tabaci and B. argentifolii (after Ren et al. 2002 ); (c) Bieri function calculated for Harmonia axyridis (solid line), Hippodamia variegata (dashed line) and Adalia bipunctata (dotted line) reared on Myzus persicae at 25° C (after Lanzoni et al. 2004 ); (d) polymodality in Chilocorus nigritus at 30° C, RH 62% and fed with Abgrallaspis cyanophylli (after Posonby & Copland 2007 ); (e) parabolic (second order power) function in Anegleis cardoni fed with Lipaphis erysimi (crosses) and long plateau of Anegleis cardoni fed with Aphis craccivora (dots; both after Omkar et al. 2009 ); (f) two levels in Harmonia axyridis at 25° C fed with Aphis fabae (after Stathas et al. 2001 ); (g) monotonous level (almost constant) in Scymnus louisianae fed with Aphis glycines (Brown et al. 2003 ); (h) bimodality in Exochomus quadripustulatus at thermoperiod 9/19° C fed with Pulvinaria regalis (Sengonca & Arnold 2003 ). 88 O. Nedveˇ d and A. Honeˇk
The length of the oviposition period is species - The fecundity of Anegleis cardoni changed with food specifi c and decreases rapidly with increasing tem- suitability: it was three times higher on Aphis gossypii perature, since longevity then decreases. The than on Lipaphis pseudobrassicae , while the oviposition oviposition period of Scymnus levaillanti lasted 87, 76, period was twice as long and the mean reproductive 47 and 32 days at 20, 25, 30 and 35° C respectively rate 1.34 times higher (Omkar et al. 2009 ). The fecun- (Uygun & Atl ı han 2000 ). No eggs were deposited at dity of C. septempunctata was 35% higher when fed 15 ° C, even though the development thresholds for with Aphis fabae reared on a susceptible cultivar of Vicia eggs and larvae were between 11 – 12 ° C. The oviposi- faba than when the aphid had been fed on a resistant tion periods of Axinoscymnus cardilobus lasted 109, 61, one (Shannag & Obeidat 2008 ). and 17 days at 17, 26 and 32 ° C, respectively (Huang A decrease in prey density (the scale Abgrallaspis et al. 2008 ). cyanophylli ) caused a signifi cant but transient decline The oviposition period may vary with food quality. in egg production in Chil. nigritus. A heterogeneous The oviposition period was 22.4 days in C. septempunc- prey population (mix of diverse developmental stages) tata fed with the cereal aphid Sitobion avenae (Rana & elicited signifi cantly higher levels of oviposition at Kakker 2000 ), but only 16 days when reared on Brevi- similar host densities than homogeneous population coryne brassicae (ElHag & Zaitoon 1996 ). In Anegleis (cohort of equally aged individuals), irrespective of cardoni, it was twice as long (58 days) on Aphis gossypii the growth stage of the prey (Ponsonby & Copland than on Lipaphis pseudobrassicae (27 days) (Omkar et al. 2007 ). 2009 ). Of fi ve generations of Cer. undecimnotata produced in While the average pre - oviposition and oviposition experimental cages during a year, the greatest numbers periods in melanic colour morph of C. septempunctata of eggs were laid by females of the fi rst and second in India were 10.2 and 68.9 days, respectively, they generations (Katsoyannos et al. 1997 ). were 14.6 and 76.9 days respectively in normal Crowding has an adverse effect on fecundity. Indi- morphs (Rhamhalinghan 1986 ). vidual females of Har. axyridis laid an average of 13 eggs per day, while females grouped as 10, 20, 30 and 40 per container laid 9, 6, 3 and 2 eggs per day, respec- 3.5.8 Fecundity tively (Abdel - Salam & Abdel - Baky 2001 ). The parasitoid Dinocampus coccinellae has been The total lifetime egg production (fecundity) is species - reported as having a great effect on the fertility of specifi c , increasing with the size of the ladybird, and mature female ladybirds. The parasitoid larva nor- dependent on temperature and on the quality and mally castrates the host ladybird and usually causes quantity of food both during the pre - imaginal devel- death. However, at relatively high temperatures (25° C), opment of the female and during reproduction. Fecun- it was found that daily numbers of coccinellid eggs dity is also infl uenced by mating frequency , age of increased during two days after parasitization and then the parents, population density , illumination, pho- gradually decreased to stop 8 – 9 days after parasitiza- toperiod , phenotype; it also changes with generation, tion. Although mortality of the females was high etc. (Table 3.1 ). It is the product of daily fecundity (ovi- (71%), half of those that survived began to oviposit position rate) and the duration of the oviposition again 12 days after the parasitoid larvae had emerged period . (Triltsch 1996 ). The relationship between food quantity and fecun- Melanic females of C. septempunctata in India laid dity or fertility is called the numerical response more eggs (302 – 412) than the females of the typical (5.3 ). The shape of the relationship is usually a convex colour morph (278 – 379) (Rhamhalinghan 1986 ). curve. In Scymnus subvillosus the numerical response In Micraspis discolor in India, fecundity was the lowest was similar to its functional response that matched at the lowest experimental temperature of 20 ° C, Holling ’ s type II (Atl ı han & G ü ldal 2009 ). A twofold highest at the optimum temperature, and decreased at increase in prey density (Aphis gossypii ) brought the highest temperature of 30° C (Omkar & Pervez about a twofold increase in lifetime oviposition and 2002 ) ( 3.6.4 ; Fig. 3.8 b). In Chil. nigritus , no oviposi- mean oviposition rate in C. septempunctata (Xia et al. tion occurred at the low temperature of 18° C. The 1999 ). lifetime fecundity increased from 20 to 24 ° C and then (a) 300 SSUB NOCU 250 DCAT ACAR 200 ABIP RLOP ENIG 150 SPUN
Longevity (d) SLEV 100 NINC NBIS 50
0 10 15 20 25 30 35 40 (b) 500 Temperature (°C) 450
400
350
300
250
200
150 Lifetime egg production 100
50
0 10 15 20 25 30 35 40 (c) 200 Temperature (°C) 180
160 0 140
120
100
80
60 Net reproduction rate R rate reproduction Net 40
20
0 (d) 10 15 20 25 30 35 40 0.20 Temperature (°C) 0.18 m
0.16
0.14
0.12
0.10
0.08
0.06
0.04
Intrinsic rate of population increase0.02 r
0.00 10 15 20 25 30 35 40 Temperature (°C)
Figure 3.8 Temperature effects on selected parameters of adult life. (a) longevity; (b) lifetime egg production; (c) net reproduction rate R0 (Andrewartha & Birch 1954 ); (d) intrinsic rate of population increase r m (Andrewartha & Birch 1954 ). Data for 12 coccinellid species: Adalia bipunctata, ABIP (Jalali et al. 2009 ); Axinoscymnus cardilobus, ACAR (Huang et al. 2008 ); Delphastus catalinae , DCAT (Kutuk & Yigit 2007 ); Diomus austrinus, DAUS, (Chong et al. 2005 ); Parexochomus nigromaculatus , ENIG (Atl ı han & Ö zg ö kce 2002 ); Clitostethus oculatus, NOCU (Ren et al. 2002 ); Nephus bisignatus, NBIS (Kontodimas et al. 2007 ); Nephus includens, NINC (Kontodimas et al. 2007 ), Lindorus lophantae, RLOP (Stathas 2000 ); Scymnus levaillanti , SLEV (Uygun & Atl ı han 2000 ); Scymnus subvillosus , SSUB (Atl ı han & Chi 2008 ); Stethorus pusillus, SPUN (Roy et al. 2003 ). 90 O. Nedveˇ d and A. Honeˇk decreased up to 30° C. No eggs were produced at 34° C. 6th and 7th generations formed the hibernating popu- However, daily fecundity was highest at 30 ° C (Pon- lation (Kontodimas & Stathas 2005 ). sonby 2009 ). Coccinella quinquepunctata , C. septempunctata and C. The reproductive output (percentage of body magnifi ca are potentially polyvoltine (Ceryngier et al. weight allocated to reproduction during 24 h) was 2004 ). Heterogeneous voltinism ( 6.2.1.6 ) appears to similar (12.5%) in large C. septempunctata and small be one of the factors responsible for the predominance P. quatuordecimpunctata (Hon eˇ k et al. 2008 ). of C. septempunctata in most habitats of the Palaearctic and for its successful invasion of the Nearctic Region (Hodek & Michaud 2008 ). The very successful invader 3.5.9 Longevity Har. axyridis regularly has two generations per year, even in colder temperate countries (Brown et al. 2008 ), 3.5.9.1 Voltinism and unlike other ladybirds even reproduces late in the season. The number of generations per year and the lifespan The lifespan of the sequential generations of poly- of ladybirds depend on the climatic conditions in the voltine species usually decreases in the laboratory, region. However, many species, even in warmer cli- probably due to inbreeding (6.2.1 ). Thus, in four suc- mates, normally have a single generation (are univol- cessive generations of Menochilus sexmaculatus longev- tine ), and live for one year including several months ity was respectively 87, 89, 63 and 50 days in males, in dormancy (also Chapter 6 ). and 111, 101, 90 and 50 days in females (Hukushima In several species, a second overwintering has been & Kouyama 1974 ). reported in a minority of individuals. Thus there are The overlap of generations in bivoltine species (such records of a second hibernation in Calvia quatuordec- as A. bipunctata in Central Europe) enables the spread imgutta (Kanervo 1946 ), in P. quatuordecimpunctata in the population of pathogens and parasites such as (Hariri 1966 ), in Stethorus pusillus (Putman 1955 ), in the mite Coccipolipus hippodamiae (Webberley et al. Aiolocaria hexaspilota (Iwata 1932 , Savoiskaya 1970 ) 2006 ; 8.3 ). and C. septempunctata (Sundby 1968 ). Savoiskaya (1970) reported that 15– 20% of a Har. axyridis 3.5.9.2 Effect of t emperature, p hotoperiod population in Kazakhstan may live and oviposit for 3 and h umidity years. Epilachna admirabilis is univoltine in northern Japan In coccinellids, as in other exotherms, life span short- and hibernates as the fi nal (fourth) instar larva. Some ens with increasing temperature. There are cases of a of the resulting adults then enter a second hibernation linear decrease of life span with temperature (3.6.4 ; together with their own larvae (Katakura 1976 ). Fig. 3.8 a). For example, the linear decrease was clear Scymnus sinuanodulus regularly lives for 2 years and in Axinoscymnus cardilobus reared at six temperatures; the fecundity is the same in both years (Lu & Mont- the longest longevity was 163 days at 17° C compared gomery 2001 ). In Pseudoscymnus tsugae the mean lon- with only 34 days at 32 ° C (Huang et al. 2008 ). Adult gevity in the laboratory was 163 and 126 days for C. novemnotata lived for 62, 48 and 21 days at 21, 27 females and males, respectively, while some individuals and 32° C, respectively (McMullen 1967 ). Olla v - nigrum of both sexes lived more than 300 days (Cheah & lived for 172 days at 15° C and only 51 days at 25° C McClure 1998 ), suggesting the potential for a 2 - year (Kreiter & Iperti 1984 ). Males of Iranian population of lifespan in the fi eld. Stethorus gilvifrons reared at various temperatures from While central European populations of Cer. undecim- 15 to 35 ° C had longest and shortest longevities of 18 notata are obligatorily univoltine (Ceryngier et al. and 13 days, and 17 and 9 days for females (Taghiza- 2004 ), at least a portion of the Cer. undecimnotata pop- deh et al. 2008 ). The longevity of this coccinellid in ulation in central Greece may complete two or more Turkey also decreased with increasing temperature overlapping generations per year under artifi cial condi- (20, 25, 30 ° C) and this was not affected by two differ- tions in shaded outdoor cages (Katsoyannos et al. ent photoperiod s (16L:8D and 8L:16D) (Aksit et al. 1997 ; 6.2.8 ). Hip. variegata may complete seven gen- 2007 ). Chil. nigritus lived for 100 – 280 days at tem- erations between April and November under artifi cial peratures of 22 – 26 ° C, 65 – 115 days at 30 ° C and only conditions in outdoor cages in Greece. Adults of the 17 – 29 days at 34 ° C (Ponsonby 2009 ). Life history and development 91
In contrast, in Col. maculata no such a clear tendency The quantity of food has inconsistent effects on lon- was recorded: longevity was 73, 74, 77, 45 and 80 gevity. Increased prey (Hyalopterus pruni ) consumption days at 19, 21, 23, 25 and 27° C, respectively (Wright did not change the longevity of Scymnus subvillosus , & Laing 1978 ). The mean adult longevities of Delphas- but did result in a higher intrinsic rate of increase tus catalinae were 40 days at a constant 30 ° C and 42 (Atl ı han & G ü ldal 2009 ). When the food provided to days at fl uctuating temperatures of 25/35 ° C Har. axyridis was limited, mean longevity increased (Kutuk & Yigit 2007 ). although mean reproductive life span and fecundity The longevity of females of Chil. nigritus increased were reduced (Agarwala et al. 2008 ). However, there with increasing relative humidity (162 days at 40%, was a difference between groups of individuals, with
220 at 80%), but net reproductive rate (R 0 ) and the one group showing a positive correlation and the other maximum intrinsic rate of increase ( rmax) were higher group a negative correlation between reproduction at the lower humidity (Senal 2006 ). and longevity.
3.5.9.3 Effect of f ood 3.5.9.4 Effect of s exual a ctivity Adult longevity tends to be longer on a more suitable Males may have a longer or shorter longevity than diet. Longevity of Anegleis cardoni was almost double females. Female Psyllobora confl uens lived 46 days, but when fed the more suitable prey Aphis gossypii than males 59 days, when fed with Erysiphe cichoracearum when fed the less suitable Lipaphis pseudobrassicae (Cividanes et al. 2007 ). In contrast, the mean longev- (Omkar et al. 2009 ). A diet of Myzus persicae increased ity of female Serangium parcesetosum was longer (71 the adult longevity and fecundity of C. undecimpunctata days) than that of males (60 days) (Al- Zyoud et al. compared with one of Aphis fabae (Cabral et al. 2006 ). 2005 ). There was no signifi cant difference between the In contrast, however, the longevity of Chil. nigritus longevities of male and female P. quatuordecimpunctata was almost twice when fed Aspidiotus nerii than Abgral- (Kalushkov & Hodek 2005 ), but in Chil. nigritus , males laspis cyanophylli , although the latter would appear are on average longer - lived than females (Ponsonby the more suitable prey since it more than doubled 2009 ). fecundity (Ponsonby 2009 ). Moreover, the adult lon- Ageing trends were sex dependent in P. dissecta , with gevities of Har. axyridis and A. bipunctata females did reproductive performance declining later in females not differ signifi cantly when reared as larvae on differ- than in males (Mishra & Omkar 2006 ). ent diets (either natural or artifi cial) and then on arti- There is a strong trade - off between the number of fi cial diet as adults (120 to141 or 74 to 118 days, matings and longevity. Longevity decreased with an respectively; Ware et al. 2008 ). The longevity of increasing number of matings in both Menochilus sex- females (59 – 76 days) and males (54 – 64 days) of P. maculatus and P. dissecta indicating a cost of mating quatuordecimpunctata was only little affected by seven (Omkar & Mishra 2005 ). Post - hibernation longevity aphid species provided as different food (Kalushkov & was much shorter (76 days) in females of Har. axyridis Hodek 2005 ). that lived with male in limited space and mated regu- The longevity of Har. axyridis fed with Aphis glycines larly than in females mated before hibernation and reared on three susceptible varieties of soybean was then maintained without a male (107 days) and also greater (12.5 days) than on three resistant varieties much shorter than in virgin females (135 days) (Fois (7.3 days) (Lundgren et al. 2009 ). In contrast, the et al. unpublished). adult longevity of C. septempunctata was not affected by whether Aphis fabae was reared on a susceptible (major) or on a partially resistant (79S4) cultivar of Vicia faba (Shannag & Obeidat 2008 ). No signifi cant differences 3.6 TEMPERATURE AND were reported in longevity or other characteristics of DEVELOPMENT Col. maculata fed with Bt- transgenic corn pollen, non- Bt pollen, or Schizaphis graminum (Ahmad et al. Finally, we provide a general account of the more 2006 ). Also P. japonica was not affected when fed with recent research on the main factor infl uencing coc- Aphis gossypii reared on either transgenic or non - cinellid development, namely temperature. Earlier transgenic cotton (Zhu et al. 2006 ). data have been reviewed by Hone ˇ k (1996) . The life of 92 O. Nedveˇ d and A. Honeˇk exotherms, with their limited capacity for thermoregu- A linear model approximates the course of devel- lation, is dependent on the external temperature. This opment rate in the ecologically relevant temperature restricts the range of conditions in which they can range and enables the calculation of two thermal con- survive, determines the rate at which life processes stants. The fi rst of these is the above - mentioned lower proceed within this range and, together with body size development threshold (LDT; Hone ˇ k & Kocourek (Gillooly et al. 2002 ), controls the fi tness of the organ- 1988 ), also known as the basal temperature Tb ism (Kingsolver & Huey 2008 ). Temperature deter- (Trudgill et al. 2005 ), and which is the temperature mines the length of development of the immature below which development ceases. The other constant stages, the length of the teneral period from adult is the sum of effective temperatures SET or, in ecdysis to fi rst oviposition, the quantity and duration of other words, the thermal time T which is the number oviposition and the length of life. The role of tempera- of day degrees [dd] above LDT for completion of a ture in survival during hibernation and aestivation is developmental stage). It has to be remembered that described in 6.4.4 . LDT is a virtual value, but it is convenient for predicting temperature effects under ecologically relevant tem- peratures. Under real conditions development is 3.6.1 Thermal constants already seriously impaired below a temperature higher than the LDT by some 2 – 4 ° C. Growth and development of pre- adult stages occur only across a specifi c range of temperature. Within this range the development time and rate of develop- 3.6.2 Relationship between LDT and SET ment (a reciprocal of development time) vary with temperature. The l ower temperature threshold is Recent results on the effects of temperature on pre- the temperature below which a particular stage of an imaginal development (Table 3.3 ) contain data for 44 animal cannot develop. After some time ( 3.6.4.1 ) it populations of 25 coccinellid species. The results dies, probably because of the loss of correlation confi rm the conclusion of the earlier review of Hon eˇ k between physiological and behavioural functions. At (1996) that coccinellids are warm- adapted species the other extreme, the range of tolerated temperature with a relatively high LDT (mostly between 9– 15 ° C; is limited by the upper temperature threshold at 17 ° C for tropical Chil. nigritus ; Ponsonby 2009 ) and a which the animal dies from heat. low SET (200 – 320 dd for total development; but over The relationship between the rate of development 500 dd for small coccidophagous species; Table 3.3 ). and temperature is linear only within the range of For the whole family Coccinellidae, the average LDT what are called the ecologically relevant tempera- calculated from Table 3.3 for eggs, larvae, pupae and tures at which most of the life activities of the animals total development, respectively, is 9.8, 9.3, 10.1 and take place. Close to the upper development limit, the 10.1 ° C and the average SET is 64, 167, 78 and 304 dd. relationship becomes non- linear, attains its highest Another plot of data for many species, both aphidopha- point at the temperature optimum where develop- gous and coccidophagous, resulted in a LDT of about ment rate is highest (i.e. development time shortest), 10 ° C (Dixon et al. 1997 ). and it then decreases sharply as the upper lethal tem- The combination of a high LDT and a low SET guar- perature limit is approached. The relationship between antees a fast development at high temperatures, in the rate of development and temperature thus typically contrast to cold adapted species whose LDT is low and has the shape of a right skewed peak, whose left slope SET high (Trudgill 1995 ). This adaptive covariance of also may divert from linearity near the lower develop- thermal constants results in a negative relationship ment threshold (Gilbert & Raworth 1996 ). Several between LDT and SET (Hone ˇ k & Kocourek 1988 ), and models which have been proposed to approximate this this also holds for data presented in this chapter (Fig. course of development rate with temperature, e.g. 3.9 ). Interpretation of this correlation is diffi cult, those of Lactin et al. (1995) and Briere et al. (1999) because the negative slope of the regression of the LDT which enable the calculation of temperature optima on the SET is both a consequence of biological varia- and upper lethal temperatures, were reviewed by Kon- tion and a statistical artefact. For a detailed discussion todimas et al. (2004) . of this matter, see Hone ˇ k (1996) . Life history and development 93 ) (1999) Continued ( (1996) (2003) (1998) (1995) (1995) (1995) (1995) 30 ° C . Development (2007) ≤ of larva, pupa and egg, Reference temperatures temperatures Total 13.6 230 Rodriguez-Saona & Miller 10.3 268 Jalali et al. (2010) 10.4 266 Jalali et al. (2010) 11.1–13.0 475 Eliopoulos et al. (2010) — — — — Pupa — — — — — — — — Larva 2.1 270.6 0.9 90.8 0.7 405 Srivastava & Omkar — — — — − — — — — Egg 8.7 50.4 10.8 121.9 11.3 50.0 10.6 224 Katsarou et al. (2005) 8.8 63.7 8.9 128.58.27.6 9.5 65.4 105.7 114.7 7.1 1.7 164.9 9.3 309.4 8.2 13.5 302 74.3 53.8 Huang et al. (2008) 7.9 6.9 289 424 Mota et al. Ren et al. (2008) (2002) 7.4 80.1 12.6 217.7 19.2 43.4 13.4 258 Kutuk & Yigit 6.9 55.2 7.86.2 52.0 56.5 7.7 9.7 180.2 119.4 9.4 9.5 86.1 81.2 8.4 9.2 314 252 Schuder et al. (2004) Schuder et al. (2004) 5.8 55.9 7.1 174.1 8.2 68.3 7.3 294 LaMana & Miller 9.9 48.4 10.2 165.3 10.8 78.8 10.2 297 Katsarou et al. (2005) 6.58.3 52.67.2 45.3 7.5 52.4 171.6 8.2 7.7 166.0 8.5 173.9 9.4 64.3 8.3 60.8 66.5 7.7 8.5 288 7.5 LaMana 271 & Miller 292 LaMana & Miller LaMana & Miller — — — — 10.7 42.8 10.6 157.4 10.8 72.9 10.4 232 Schanderl et al. (1985) 12.4 65.4 13.9 156.9 14.4 55.4 14.3 266 Chong et al. (2005) 10.2 47.0 10.9 162.9 10.9 69.2 10.8 279 LaMana & Miller 11.5 39.8 13.3 108.8 12.1 67.6 12.6 218 Jalali et al. (2009) 12.9 64.9 13.0 135.7 14.8 51.5 13.9 240 Chong et al. (2005) 10.4 44.0 11.4 114.0 11.7 71.1 11.2 232 Jalali et al. (2009a) 11.9 39.2 9.3 148.4 11.2 73.0 10.8 254 Jalali et al. (2009a) 13.9 88.3 16.2 241.8 13.4 79.0 15.6 363 Ponsonby & Copland 11.4 34.5 5.9 166.1 10.7 67.8 9.4 246 Olszak (1987) LDT SET LDT SET LDT SET LDT SET
† † † †
* * * * * * *
* * Thermal constants, lower development threshold LDT ( ° C ) and sum of effective temperatures SET (dd) for the development SET ) and sum of temperatures effective C ° ( LDT threshold development Thermal constants, lower Hippodamia convergens Hippodamia convergens Harmonia axyridis Adalia bipunctata Diomus austrinus Adalia bipunctata Harmonia axyridis Adalia bipunctata Axinoscymnus cardilobus Delphastus catalinae Calvia quatuordecimguttata Calvia quatuordecimguttata Chilocorus bipustulatus Clitostethus arcuatus Clitostethus oculatus Coccinella septempunctata Diomus austrinus Adalia bipunctata Calvia quatuordecimguttata Chilocorus nigritus Coccinella septempunctata Table 3.3 Adalia bipunctata Adalia bipunctata Adalia bipunctata Calvia quatuordecimguttata total pre - adult development. Calculated using a linear model of Calculated of and data adult development. relationship vs. temperature rate the development - total pre time of the prepupae included in larval stage. Adalia bipunctata 94 O. Nedveˇ d and A. Honeˇk (2001) (1996) (1988) (2002) (2001) (1998) (2004) (2008) ıhan (2000) Lu & Montgomery Reference — Total 9.3 513 Kontodimas et al. (2007) 10.6 657 M’Hamed & Chemseddine 10.9 408 Kontodimas et al. (2007) 11.7 159 Raworth (2001) — — — — Pupa — — — — 12.8 56.2 13.5 242 Cividanes & Gutierrez — — — — — Larva 8.1 260.5 1.4 231.7 — — — — — — — — — — Egg 6.3 77.4 15.1 65.9 6.3 72.4 11.3 201 Allawi (2006) 9.0 46.2 11.9 133.1 12.5 45.8 11.4 220 Kreiter (1985) 9.8 66.1 5.5 136.4 11.9 138.0 5.5 329 Atlıhan & Chi 1.2 58.7 4.2 176.2 3.2 65.4 3.6 299 Omkar & Pervez 8.77.9 114.0 132.9 8.0 8.0 240.4 262.4 8.3 8.0 90.0 100.7 8.2 8.3 444 419 Stathas (2000) Stathas et al. (2002) — — — — — 13.7 28.1 — 16.0 41.1 7.9 119.1 7.9 102.4 11.5 236 Allawi (2006) 10.711.8 95.9 12.8 64.6 140.2 8.2 13.6 142.5 62.7 10.7 88.8 12.6 10.0 295 Cheah & McClure 296 Uygun & Atl 10.0 77.8 10.9 138.0 10.9 69.7 10.7 285 Grafton-Cardwell et al. (2005) 16.4 100 8.4 274 9.2 116.0 11.9 469 Izhevsky & Orlinsky 11.5 61.5 11.4 102.5 11.0 52.1 11.4 215 Roy et al. (2002) 17.0 26.1 14.2 118.0 14.6 69.0 14.9 210 dos Santos (1992) 11.8 101.9 10.4 196.8 11.1 103.8 11.0 403 Kontodimas et al. (2004) 12.612.8 51.9 50.4 12.3 12.4 102.8 99.9 12.4 12.4 42.5 42.3 12.4 12.5 197 193 Mori et al. (2005) Mori et al. (2005) 11.5 57.7 7.9 140.4 6.6 89.7 8.8 284 Atlıhan & Ozgokce 12.1 103.1 8.2 269.7 10.6 102.5 9.3 512 Kontodimas et al. (2004) LDT SET LDT SET LDT SET LDT SET
)
* * ‡ ‡
Continued ( -nigrum different geographic populations. sex differences. Scymnus sinuanodulus Scymnus levaillanti Scymnus marinus Scymnus syriacus Stethorus japonicus Scymnus levaillanti Nephus includens Olla v Scymnus subvillosus Nephus reunioni Rodolia cardinalis Sasajiscymnus tsugae Stethorus pusillus Stethorus japonicus Stethorus pusillus * different food type. Nephus includens Scymnus argentinicus Propylea dissecta Table 3.3 Nephus bisignatus Parexochomus nigromaculatus † ‡ Lindorus lophanthae Lindorus lophanthae Lindorus lophanthae Nephus bisignatus Life history and development 95
15
13
11 LDT (°C) 9
7
5 25 50 75 100 125 SET (dd)
Figure 3.9 Lower development threshold LDT plotted against sum of effective temperatures SET in pupae of 32 species of coccinellid listed in Table 3.3 (data for three outlier species excluded). LDT = 14.7 − 0.0553 SET, R 2 = 0.239, P < 0.005.
3.6.3 Thermal window and development rate isomorphy was demonstrated for 243 (57%) of the rate isomorphy populations and any violation of this principle in the rest of the species was very small. The existence of Two recent developments have provided rules that the ‘ thermal window ’ and ‘ development rate isomor- govern the temperature relationships of different phy ’ was tested and demonstrated to be true for a species. A meta - analysis of data for many insect species number of coccinellid species (Jarosik et al. 2002 ). has revealed that the span between the LDT and the optimum temperature for each individual species is about 20 ° C, regardless of whether the species are 3.6.4 Other events affected by temperature adapted to cold (i.e. have a low LDT) or warm condi- tions (Dixon et al. 2009 ). The existence of this thermal The prevailing temperature during pre- adult develop- window, an intrinsic limit on thermal requirements, ment infl uences adult body size but its effect is diffi cult stresses the necessity of adaptation to the thermal con- to separate from the effect of the rate of food consump- ditions prevailing in the geographic area and in the tion. Recent results from Diomus austrinus (Chong et al. ecological niche inhabited by the population. Another 2005 ) and Aphidecta obliterata (Timms & Leather 2008 ) study (Jarosik et al. 2002 ) revealed that, in a popula- were ambiguous, since temperature affected the body tion of any particular species, the LDT of the egg, larva weight of males and females in a different way in the and pupa is, in fact, identical and any experimentally two species. established differences are probably caused by an Temperature further determines the course of events observational bias. As a result, each developmental of adult life. The thermal requirements for completing stage takes a constant proportion of the total develop- teneral development , i.e. the time from moult to ment time and this proportion of development time adult to the fi rst oviposition, can also be approximated does not change with temperature. This phenomenon by a linear relationship between development rate and was called development rate isomorphy and was temperature, but of course only if dormancy does not tested with 426 populations belonging to 342 species take place. The average threshold temperature LDT cal- of insects and mites. In a rigorous test, development culated from data in Table 3.4 (without the outlier at 96 O. Nedveˇ d and A. Honeˇk
Table 3.4 Thermal constants, lower development et al. 2008 ). While R0 was highest (130) at 26° C and threshold LDT (° C ) and sum of effective temperatures SET lower at both lower (22° C, 115) and higher tempera- (dd) for teneral pre- oviposition period. Calculated using a tures (30 ° C, 82), r m was greatest at the highest tem- linear model of development rate vs. temperature perature in Chil. nigritus (Ponsonby 2009 ). relationship, and data of temperatures ≤ 30 ° C .
Species LDT SET Reference 3.6.4.1 Tolerance to e xtreme t emperatures Adalia bipunctata* 10.9 69.1 Jalali et al. (2009) Adalia bipunctata* 1.3 142.4 Jalali et al. (2009) The supercooling point (SCP; Chapter 6 ) is naturally Axinoscymnus 7.8 127.4 Huang et al. (2008) low for non - feeding stages, i.e. eggs and pupae, and cardilobus high for larvae and adults. The mean SCP of Har. Clitostethus 5.1 317.3 Ren et al. (2002) axyridis eggs was − 27 ° C, and − 21 ° C for pupae , while oculatus it was − 14 ° C for larvae and − 1.9 ° C for adults (Koch Delphastus 10.9 93.0 Kutuk & Yigit (2007) et al. 2004 ). The mean SCP of fresh eggs of C. septem- catalinae punctata was − 27 ° C and for older eggs it was − 24.5 ° C, Nephus bisignatus 10.0 102.1 Kontodimas et al. probably due to accumulation of metabolic water in (2004) the embryo (Nedv eˇ d 1994 ). Wild - collected pupae of C. Nephus includens 10.7 86.5 Kontodimas et al. septempunctata in June and July had a SCP of − 19 ° C. (2004) Olla v-nigrum 13.5 138.8 Kreiter (1985) The mean SCP increased during larval development in − Scymnus 10.9 93.0 Atlıhan & Chi (2008) Cer. undecimnotata (Nedv eˇ d 1994 ): from 20 ° C in the subvillosus second instar, through −16 ° C in the third , to − 9 ° C in the fourth instar. In contrast, older and larger fourth * different food type. instar larvae of Exochomus quadripustulatus had a lower SCP ( −17 ° C) than smaller larvae of the same instar (− 10 ° C) (Nedv eˇ d 1994 ). 1.3° C LDT) is 9.5° C, which is similar to the LDT for The survival of third and fourth instar larvae of C. immature stages. The average sum of effective tem- undecimpunctata was higher than that of fi rst and perature SET for teneral development is 127 dd. second instars when exposed to 6° C for a week. Larval Further important effects of temperature concern survival declined sharply after 15 days. There was only reproduction . Temperature infl uences longevity , 25% adult emergence from pupae chilled for 30 days. the number of eggs laid and the distribution of oviposi- Adults survived the extended periods of cold storage tion through adult life. The data for nine species (Fig. better than the other developmental stages (Abdel - 3.8 ) reveal a uniform trend. Mean longevity decreases Salam & Abdel - Baky 2000 ). monotonically with increasing temperature (Fig. 3.8 a) Adults and second instar larvae of Har. axyridis were but the production of eggs peaks at around 25° C (Fig. heat stressed at 35 ° C, and showed high mortality at 3.8 b). Using the distribution of mortality and oviposi- 40° C, but these hot conditions were tolerated by all tion in time, it is possible to calculate the innate other stages (Acar et al. 2004 ). In our experiments capacity for increase, which also depends on tem- with Har. axyridis (Fois & Nedv eˇ d, unpublished), 100% perature, of a coccinellid population (for details see e.g. mortality occurred in the egg and pupal stages at Andrewartha & Birch 1954 ). 35 ° C. The supercooling point (− 17 ° C) and lower lethal Parameters of offspring production, net reproduc- temperature (− 16.7 ° C) remained relatively constant tion rate R 0 (Fig. 3.8 C) and intrinsic rate of popu- for the overwintering populations in the outdoor hiber- lation increase rm (Fig. 3.8 d) are also temperature naculum. In contrast, the supercooling point and sensitive and peak between 25 – 30 ° C as in P. japonica , lower lethal temperature of the population overwinter- where the highest rm of 0.113 occurred at 25° C (Chi & ing indoors clearly increased as the winter progressed,
Yang 2003 ). In Stethorus pusillus, the rm followed a from − 18.5 to − 13.2 ° C and − 16.7 to − 14.1 ° C, respec- typical asymmetrical dome- shape pattern, as tempera- tively (Berkvens et al. 2010 ). ture increased, with maximum values of 0.196 per day The lower and upper thresholds for survival for 24 at 30° C (Roy et al. 2003 ). Nevertheless, there exist hours of Delphastus catalinae were around 0 and 40° C, warm- adapted species like Stethorus gilvifrons (Mulsant) respectively. Survival of their pupae was similar to that whose fecundity, R 0 and r m peak at 35 ° C (Taghizadeh of adults (Simmons & Legaspi 2004 ). The fi rst three Life history and development 97 instars of Scymnus marinus had an optimum tem- specifi c Cry3Bb1 protein for corn rootworm control on perature for development of 30° C; they also devel- aboveground insect predators . J. Econ. Entomol. 99 : oped at 35 ° C but all died at 40 ° C. In contrast, the 1085 – 1095 . fourth instar larvae, prepupae and pupae of this species Aksit , T. , I. Cakmak and G. Ozer . 2007 . Effect of temperature did develop at 40 ° C, although at a slower rate. The and photoperiod on development and fecundity of an acarophagous ladybird beetle, Stethorus gilvifrons . Phy- temperature optimum in these stages remained 30 ° C toparasitica 35 : 357 – 366 . (M ’ Hamed & Chemseddine 2001 ). Allawi , T. F. 2006 . Biological and ecological studies on In conclusion, coccinellids are average athletes in Scymnus syriacus and Scymnus levaillanti (Coleoptera: Coc- the wrestling match that Life has with Ambient Tem- cinellidae) . Eur. J. Entomol. 103 : 501 – 503 . perature. Within the range of performance of insects, Alvarez - Alfageme , F. , N. Ferry , P. Castanera , F. Ortego and A. coccinellids are no extremophiles; they do not live in M. R. Gatehouse . 2008 . Prey mediated effects of Bt maize particularly cold or warm conditions – or at least no on fi tness and digestive physiology of the red spider mite such species have as yet been discovered. predator Stethorus punctillum Weise (Coleoptera: Coccinelli- dae) . Transgenic Res. 17 : 943 – 954 . Al - Zyoud , F. , P. Blaeser and C. Sengonca , 2005 . Investigations ACKNOWLEDGEMENTS on the biology and prey consumption of the predator Seran- gium parcesetosum Sicard (Coleoptera: Coccinellidae) by feeding on Trialeurodes vaporariorum Westwood (Hom- AH ’ s contribution to this chapter was supported by optera: Aleyrodidae) as prey. J. Plant Dis. Prot. 112 : grant #522/08/1300 of the Grant Agency of the 485 – 496 . Czech Republic. Anderson , J. M. E. 1981 . Biology and distribution of Scym- nodes lividigaster (Mulsant) and Leptothea galbula (Mulsant) Australian Lady birds (Coleoptera: Coccinellidae) . Proc. REFERENCES Linn. Soc. N.S.W. 105 : 1 – 15 . Andrewartha , H. G. and L. C. Birch . 1954 . The distribution and Abdel - Salam , A. H. and N. F. Abdel - Baky . 2000 . Possible abundance of animals . The University of Chicago Press , storage of Coccinella undecimpunctata (Col., Coccinellidae) Chicago . under low temperature and its effect on some biological Anonymous . 1997 . Biological control of aphids in WANA characteristics . J. Appl. Entomol. 124 : 169 – 176 . using coccinellids . Annual Report , Icarda, Syria. p. 8 . Abdel - Salam , A. H. and N. F. Abdel - Baky . 2001 . Life table and Arakaki , N. 1988 . Egg protection with faeces in the lady - biological studies of Harmonia axyridis Pallas (Col.: Coc- beetle, Pseudoscymnus kurohime (Miyatake) (Coleoptera: cinellidae) reared on the grain moth eggs of Sitotroga cere- Coccinellidae) . Appl. Entomol. Zool. 23 : 495 – 497 . alella Olivier (Lep., Gelechiidae) . J. Appl. Entomol. 125 : Atl ı han , R. and H. Chi . 2008 . Temperature - dependent devel- 455 – 462 . opment and demography of Scymnus subvillosus (Coleop- Abdel - Salam , A. H. , J. J. Ellington , M. A. El - Adl , A. M. Abou tera: Coccinellidae) reared on Hyalopterus pruni (Homoptera: El- Naga and A. A. Ghanim . 1997 . Longevity and fecundity Aphididae) . J. Econ. Entomol. 101 : 325 – 333 . of Harmonia axyridis adults reared on an artifi cial diet and Atl ı han , R. and M. S. Ö zg ö kce . 2002 . Development, fecundity pink bollworm eggs. 1st National Conference, Mansouri 1 : and prey consumption of Exochomus nigromaculatus feeding 50 – 57 . on Hyalopterus pruni . Phytoparasitica 30 : 443 – 450 . Acar , E. B. , D. D. Mill , B. N. Smith , L. D. Hansen and G. M. Atl ı han , R. and H. G ü ldal . 2009 . Prey density - dependent Booth . 2004 . Calorespirometric determination of the feeding activity and life history of Scymnus subvillosus . Phy- effects of temperature on metabolism of Harmonia axyridis toparasitica 37 : 35 – 41 . (Col: Coccinellidae) from second instars to adults. Environ. Attygalle , A. B. , S. R. Smedley , T. Eisner and J. Meinwald . Entomol. 33 : 832 – 838 . 1996 . Tocopheryl acetates from the pupal exocrine secre- Agarwala , B. K. , H. Yasuda and S. Sato . 2008 . Life history tion of the squash beetle, Epilachna borealis (Coccinellidae) . response of a predatory ladybird, Harmonia axyridis (Pallas) Experientia 52 : 616 – 620 . (Coleoptera: Coccinellidae), to food stress. Appl. Entomol. Banken , J. A. O. and J. D. Stark . 1997 . Stage and age infl u- Zool. 43 : 183 – 189 . ence on the susceptibility of Coccinella septempunctata Ahmad , R. 1970 . Studies in West Pakistan on the biology of (Coleoptera: Coccinellidae) after direct exposure to one nitidulid species and two coccinellid species (Coleop- Neemix, a neem insecticide. J. Econ. Entomol. 90 : tera) that attack scale - insects (Hom., Coccoidea) . Bull. 1102 – 1105 . Entomol. Res. 60 : 5 – 16 . Banks , C. J. 1955 . An ecological study of Coccinellidae (Col.) Ahmad , A. , G. E. Wilde , R. J. Whitworth and G. Zolnerowich . associated with Aphis fabae Scop. on Vicia faba . Bull. 2006 . Effect of corn hybrids expressing the coleopteran- Entomol. Res. 46 : 561 – 587 . 98 O. Nedveˇ d and A. Honeˇk
Banks , C. J. 1956 . Observations on the behaviour and mortal- Aphididae) and Aleyrodes proletella (Homoptera: Aleyrodi- ity in Coccinellidae before dispersal from egg - shells . Proc. dae) as prey for Coccinella undecimpunctata (Coleoptera: Coc- Roy. Entomol. Soc. London A 31 : 56 – 60 . cinellidae) . Biol. Control 39 : 434 – 440 . Baskaran , R. K. and K. Suresh . 2006 . Comparative biology Camarano , S. , A. Gonzalez and C. Rossini . 2006 . Chemical and predatory potential of black beetle, Chilocorus nigrita defense of the ladybird beetle Epilachna paenulata . Chem- (Fab.) on three scale insects. J. Entomol. Res. 30 : 159 – 64 . oecology 16 : 179 – 184 . Baungaard , J. and M. H ä m ä l ä inen . 1981 . Notes on egg - batch Ceryngier , P. , J. Havelka and I. Hodek . 2004 . Mating and size in Adalia bipunctata L. (Col.: Coccinellidae) . Ann. activity of gonads in pre - dormant and dormant ladybirds Entomol. Fenn. 41 : 25 – 27 . (Coleoptera: Coccinellidae) . Invert. Reprod. Dev. 45 : Berkvens , N. , J. Bonte , D. Berkvens et al. 2008a . Pollen as an 127 – 135 . alternative food for Harmonia axyridis . BioControl 53 : Chazeau , J. 1981 . La lutte biologique contre la conchinelle 201 – 210 . transparente du cocotier Temnaspidotus destructor (Signo- Berkvens , N. , J. Bonte , D. Berkvens , L. Tirry and P. De Clercq . ret) aux Nouvelles Hebrides (Homoptera, Diaspididae) . 2008b . Infl uence of diet and photoperiod on development Cahiers ORSTM, Serie Biologique 44 : 11 – 22 . and reproduction of European populations of Harmonia Cheah , C. A. S. J. and M. S. McClure . 1998 . Life history axyridis (Pallas) (Coleoptera: Coccinellidae). BioControl 53 : and development of Pseudoscymnus tsugae (Coleoptera: 211 – 221 . Coccinellidae), a new predator of the hemlock wooly Berkvens , N. , J. S. Bale , D. Berkvens , L. Tirry and P . De Clercq . adelgid (Homoptera: Adelgidae) . Env. Entomol. 27 : 2010 . Cold tolerance of the harlequin ladybird Harmonia 1531 – 1536 . axyridis in Europe. J. Insect Physiol. 56 : 438 – 444 . Chen , Z. H. , E. Y. Chen and F. S. Yan . 1980 . Effects of diets on Bieri , M. , J. Baumgartner , G. Bianchi , V. Delucchi and R. von the feeding and reproduction of Coccinella septempunctata L. Arx . 1983 . Development and fecundity of pea aphid Acta Entomol . Sinica 23 : 141 – 148 . (In Chinese with English (Acyrthosiphon pisum Harris) as affected by constant tem- summary.) peratures and by pea varieties . Mitt. Schweiz. Ent. Ges. 56 : Chen , F. J. , F. Ge and M. N. Parajulee . 2005 . Impact of elevated
163 – 171 . CO2 on tri- trophic interaction of Gossypium hirsutum , Aphis Bind , R. B. 2007 . Reproductive behaviour of a generalist gossypii, and Leis axyridis . Env. Entomol. 34 : 37 – 46 . aphidophagous ladybird beetle Cheilomenes sexmaculata Chi , H. and T. C. Yang . 2003 . Two sex - life table and predation (Coleoptera: Coccinellidae). Internat. J. Trop. Insect Sci. 27 : rate of Propylea japonica Thunberg (Coleoptera: Coccinelli- 78 – 84 . dae) fed on Myzus persicae Sulzer (Homoptera: Aphididae) . Birch , L. C. 1948 . The intrinsic rate of natural increase of an Env. Entomol. 32 : 327 – 333 . insect population. J. Anim. Ecol. 17 : 15 – 26 . Chong , J. H. , R. D. Oetting and L. S. Osborne . 2005 . Develop- Blackman , R. L. 1965 . Studies on specifi ty in Coccinellidae. ment of Diomus austrinus Gordon (Coleoptera: Coccinelli- Annals Appl. Biol. 56 : 336 – 338 . dae) on two mealybug prey species at fi ve constant Blackman , R. L. 1967 . The effects of different aphid foods on temperatures . Biol. Control 33 : 39 – 48 . Adalia bipunctata L. and Coccinella 7 - punctata L . Annals Cividanes , T. M. S. , F. J. Cividanes and B. D. de Matos . 2007 . of Applied Biology 59 : 207 – 219 . Biology of Psyllobora confl uens fed with Erysiphe cichora- Bonte , M. , M. A. Samih and P . De Clercq . 2010 . Development cearum fungus . Pesquisa Agropecuaria Brasileira 42 : and reproduction of Adalia bipunctata on factitious and arti- 1675 – 1679 . fi cial foods. BioControl 55 : 485 – 492 . Cividanes , F. J. and A. P. Gutierrez . 1996 . Modelling the age - Briere , J. F. , P. Pracros , A. Y. LeRoux and J. S. Pierre . 1999 . A specifi c per capita growth and reproduction of Rhyzobius novel model of temperature dependent development for lophanthae (Blaisd) (Coleoptera: Coccinellidae) . Ento- arthropods . Env. Entomol. 27 : 94 – 101 . mophaga 41 : 257 – 266 . Brown , G. C. , M. J. Sharkey and D. W. Johnson . 2003 . Bionom- Collyer , E. 1964 . Phytophagous mites and their predators ics of Scymnus (Pullus ) louisianae J. Chapin (Coleoptera: Coc- in New Zealand orchards. N. Z. J. of Agric. Res. 7 : cinellidae) as a predator of the soybean aphid, Aphis glycines 551 – 568 . Matsumura (Homoptera: Aphididae) . J. Econom. Entomol. Creed , E. R. 1975 . Melanism in the two spot ladybird: the 96 : 21 – 24 . nature and intensity of selection . Proc. R. Soc. London B. Brown , P. M. J. , H. E. Roy , P. Rothery et al. 2008 . Harmonia 190 : 135 – 148 . axyridis in Great Britain: analysis of the spread and distri- Dixon , A. F. G. 2000 . Insect Predator – Prey Dynamics: Ladybird bution of a non- native coccinellid. BioControl 53 : 55 – 67 . Beetles and Biological Control. Cambridge University Press, Buntin , L. A. and G. Tamaki . 1980 . Bionomics of Scymnus Cambridge, UK. 258 pp. marginicollis (Coleoptera: Coccinellidae). Can. Entomol. 112 : Dixon , A. F. G. and Y. Guo . 1993 . Egg and cluster - size in lady- 675 – 680 . bird beetles (Coleoptera, Coccinellidae) – the direct and Cabral , S. , A. O. Soares , R. Moura and P. Garcia . 2006 . Suit- indirect effects of aphid abundance . Eur. J. Entomol. 90 : ability of Aphis fabae , Myzus persicae (Homoptera: 457 – 463 . Life history and development 99
Dixon , A. F. G. , J. L. Hemptinne and P. Kindlmann . 1997 . Fomenko , R. B. and V. A. Zaslavskii . 1970 . Genetics of gre- Effectiveness of ladybirds as biological control agents: pat- garious beaviour in Chilocorus bipustulatus L. (Coleoptera, terns and processes. Entomophaga 42 : 71 – 83 . Coccinellidae) . Dokl. Akad. Nauk SSSR 192 : 229 – 231 . (In Dixon , A. F. G. , A. Hon eˇ k , P. Keil et al. 2009 . Relationship Russian.) between the maximum and minimum thresholds for devel- Francis , F. , E. Haubruge , P. Hastir and C. Gaspar . 2001 . Effect opment in insects. Funct. Ecol. 23 : 257 – 264 . of aphid host plant on development and reproduction of Dobzhansky , F. G. 1924 . Die weiblichen Generationsorgane the third trophic level, the predator Adalia bipunctata (Cole- der Coccinelliden als Artmerkmal betrachtet (Col.). optera: Coccinellidae) . Environ. Entomol. 30 : 947 – 952 . Entomol. Mitteilungsbl. 13 : 18 – 27 . Fujiyama , N. , C. Torii , M. Akabane and H. Katakura . 2008 . Dobrzhansky , F. G. 1926 . Genital apparatus of ladybirds as Oviposition site selection by herbivorous beetles: a compari- individual and group character . Trans. Acad. Sci. USSR 6, son of two thistle feeders, Cassida rubiginosa and Henosepil- Series 20 : 1385 – 1393 ; 1555 – 1586 . (In Russian.) achna niponica . Entomol. Exp. Appl. 128 : 41 – 48 . Dorge , S. K. , V. P. Dalaya and A. G. Pradhan . 1972 . Studies on Gage , J. H. 1920 . The larvae of the Coccinellidae . Illinois Biol. two predatory coccinellid beetles, Pharoscymnus horni Monogr. 6 : 232 – 294 . Weise and Chilocorus nigritus Fab., feeding on sugarcane Gannon , A. J. and C. E. Bach . 1996 . Effects of soybean tri- scales, Aspidiotus glomeratus G. Labdev . J. Sci. Technol. ( B) chome density on Mexican bean beetle (Coleoptera: Coc- 10 : 138 – 141 . cinellidae) development and feeding preference. Env. Duan , J. J. , G. Head , M. J. McKee et al. 2002 . Evaluation of Entomol. 25 : 1077 – 1082 . dietary effects of transgenic corn pollen expressing Gao , F. , S. R. Zhu , Y. C. Sun et al. 2008 . Interactive effects of
Cry3Bb1 protein on a non- target ladybird beetle, Coleome- elevated CO2 and cotton cultivar on tri - trophic interaction gilla maculata . Entomol. Exp. Appl. 104 : 271 – 280 . of Gossypium hirsutum , Aphis gossyppii, and Propylaea Durska , E. , P. Ceryngier and R. H. L. Disney . 2003 . Phalacro- japonica . Env. Entomol. 37 : 29 – 37 . tophora beuki (Diptera: Phoridae), a parasitoid of ladybird Gautam , R. D. 1990 . Mass - multiplication technique of coc- pupae (Coleoptera: Coccinellidae) . Eur. J. Entomol. 100 : cinellid predator, ladybird beetle ( Brumoides suturalis ) . 627 – 630 . Indian J. Agric. Sci. 60 : 747 – 750 . ElHag , E. T. A. and A. A. Zaitoon . 1996 . Biological parameters Geyer , J. W. C. 1947 . A study of the biology and ecology of for four coccinellid species in Central Saudi Arabia. Biol. Exochomus fl avipes Thunb. (Coccinellidae, Coleoptera). J. Control 7 : 316 – 319 . Entomol. Soc. South Afr. 9 : 219 – 234 ; 10 : 64 – 109 . El - Heneidy , A. H. , A. A. Hafez , F. F. Shalaby and I. A. B. El - Din . Ghanim , A. E. B. , B. Freier and T. Wetzel . 1984 . Zur Nahrung- 2008 . Comparative biological aspects of the two coccinellid saufnahme und Eiablage von Coccinella septempunctata L. species; Coccinella undecimpunctata L. and Hippodamia con- bei unterschiedlichem Angebot von Aphiden der Arten vergens Guer. under laboratory conditions . Egypt. J. Biol. Macrosiphum avenae (Fabr.) und Rhopalosiphum padi (L.) . Pest Control 18 : 51 – 59 . Arch. Phytopathol. Pfl sch. 20 : 117 – 125 . Ellingsen , I - .J. 1969 . Fecundity, aphid consumption and sur- Gibson , R. L. , N. C. Elliott and P. Schaefer . 1992 . Life history vival of the aphid predator Adalia bipunctata L. (Col., Coc- and development of Scymnus frontalis (Fabricius) (Coleop- cinellidae) . Norsk. Entomol. Tidsskr. 16 : 91 – 95 . tera: Coccinellidae) on four species of aphid. J. Kans. Eliopoulos , P. A. , D. C. Kontodimas and G. J. Stathas . 2010 . Entomol. Soc. 65 : 410 – 415 . Temperature - dependent development of Chilocorus bipustu- Gilbert , N. and D. A. Raworth . 1996 . Insects and temperature - a latus (Coleoptera: Coccinellidae). Environ. Entomol. 39 : general theory. Can. Entomol. 128 : 1 – 13 . 1352 – 1358 . Giles , K. L. , R. D. Madden , R. E. Stockland , M. E. Payton Evans , E. W. , D. R. Richards and A. Kalaskar . 2004 . Using food and J. W. Dillwith . 2002 . Host plants affect predator for different purposes: female responses to prey in the pred- fi tness via the nutritional value of herbivore prey: investiga- ator Coccinella septempunctata L. (Coleoptera: Coccinelli- tion of a plant – aphid – ladybeetle system . BioControl 47 : dae) . Ecol. Entomol. 29 : 27 – 34 . 1 – 21 . Ferrer , A. , A. F. G. Dixon and J. L. Hemptinne . 2008 . Prey Gillooly , J. F. , E. L. Charnov , G. B. West , V. M. Savage and J. H. preference of ladybird larvae and its impact on larval mor- Brown . 2002 . Effects of size and temperature on develop- tality, some life- history traits of adults and female fi tness . mental time. Nature 417 : 70 – 73 . Bull. Isectology 61 : 5 – 10 . Grafton - Cardwell , E. E. , P. Gu and G. H. Montez . 2005 . Effects Fitzgerald , D. V. 1953 . Review of the biological control of of temperature on development of vedalia beetle, Rodolia coccids on coconut palms in the Seychelles. Bull. Entomol. cardinalis (Mulsant) . Biol. Contr. 32 : 473 – 478 . Res. 44 : 405 – 413 . Greathead , D. J. and R. D. Pope . 1977 . Studies on the biology Fomenko , R. B. 1970 . The effect of aggregations of preimagi- and taxonomy of some Chilocorus spp. (Coleoptera: Coc- nal stages of Chilocorus bipustulatus L. (Coleoptera, Coc- cinellidae) preying on Aulacaspis spp. (Hemiptera: Diaspidi- cinellidae) on the duration of their development . Entomol. dae) in East Africa, with the description of a new species. Obozr. 49 : 264 – 269 . (In Russian.) Bull. Entomol. Res. 67 : 259 – 270 . 100 O. Nedveˇ d and A. Honeˇk
Gupta , A. K. , S. Srivastava , G. Mishra , K. Singh and Omkar . Hirai , Y. , H. Kobayashi , T. Koizumi and H. Katakura . 2006 . 2006 . Survival, development and life tables of two conge- Field - cage experiments on host fi delity in a pair of sympat- neric ladybirds in aphidophagous guilds . Insect Sci. 13 : ric phytophagous ladybird beetles. Entomol. Exp. Appl. 118 : 119 – 126 . 129 – 135 . Haddrill , P. R. , D. M. Shuker , S. Mayes and M. E. N. Majerus . Hodek , I. 1958 . Infl uence of temperature, relative humidity 2007 . Temporal effects of multiple mating on components and photoperiodicity on the speed of development of Coc- of fi tness in the two- spot ladybird, Adalia bipunctata (Cole- cinella septempunctata L . Acta. Soc. Entomol. Cechoslov. Praha optera: Coccinellidae). Eur. J. Entomol. 104 : 393 – 398 . 55 : 121 – 141 . Haddrill , P. R. , F. M. Waldron and B. Charles . 2008 . Elevated Hodek , I. 1996a . Dormancy . In I. Hodek and A. Hon eˇ k (eds). levels of expression associated with regions of the Dro- Ecology of Coccinellidae . Kluwer Academic Publishers , Dor- sophila genome that lack crossing over . Biol. Lett. 4 : drecht . pp. 239 – 318 . 758 – 761 . Hodek I. 1996b . Food relationships . In: I. Hodek and A. Hon eˇ k H ä m ä l ä inen , M. and M. Markkula . 1977 . Cool storage of Coc- (eds.): Ecology of Coccinellidae. Kluver Academic Publishers, cinella septempunctata and Adalia bipunctata (Col.: Coccinelli- Dordrecht . pp. 143 – 238 . dae) eggs for use in the biological control in greenhouses. Hodek , I. and P. Ceryngier . 2000 . Sexual activity in Coccinel- Ann. Agric. Fen. 16 : 132 – 136 . lidae (Coleoptera): a review . Eur. J. Entomol. 97 : 449 – Hariri , G. E. 1966 . Changes in metabolic reserves of three 456 . species of aphidophagous Coccinellidae (Coleoptera) during Hodek , I. and V. Landa . 1971 . Anatomical and histological metamorphosis . Entomol. Exp. Appl. 9 : 349 – 358 . changes during dormancy in two Coccinellidae. Ento- Harmon , J. P , A. Hayden and D. A. Andow . 2008 . Absence mophaga 16 : 239 – 251 . makes the heart grow fonder: Isolation enhances the fre- Hodek , I. and J. P. Michaud . 2008 . Why is Coccinella septem- quency of mating in Coleomegilla maculata (Coleoptera: Coc- punctata so successful? (A point - of - view) . Eur. J. Entomol. cinellidae) . J. Insect. Behav. 21 : 495 – 504 . 105 : 1 – 12 . Hattingh , V. and M. J. Samways . 1994 . Physiological and Hon eˇ k , A. 1990 . Seasonal changes in fl ight activity of Coc- behavioural characteristics of Chilocorus spp. (Coleoptera: cinella septempunctata L. (Coleoptera, Coccinellidae). Acta Coccinellidae) in the laboratory relative to effectiveness Entomol. Bohemoslov. 87 : 336 – 341 . in the fi eld as biocontrol agents. J. Econ. Entomol. 87 : Hon eˇ k , A. 1996 . Life history and development . In I. Hodek 31 – 38 . and A. Hon eˇ k (eds). Ecology of Coccinellidae . Kluwer Aca- Hawkes , O. A. M. 1920 . Observations on the life history, demic Publishers , Dordrecht . pp. 61 – 93 . biology and genetics of the ladybird beetle Adalia bipunctata Hon eˇ k , A. and F. Kocourek . 1988 . Thermal requirements for (L.) . Proc. Zool. Soc. London 78 : 475 – 490 . development of aphidophagous Coccinellidae (Coleoptera), Hazzard , R. V. and D. N. Ferro . 1991 . Feeding responses of Chrysopidae, Hemerobiidae (Neuroptera), and Syrphidae adult Coleomegilla maculata (Col.: Coccinellidae) to eggs of (Diptera): some general trends. Oecologia 76 : 455 – 460 . Colorado potato beetle (Col.: Chrysomelidae) and green Hon eˇ k , A. and F. Kocourek . 1990 . Temperature and develop- peach aphids (Homoptera: Aphididae). Environ. Entomol. ment time in insects: a general relationship between 20 : 644 – 651 . thermal constants. Zoologische Jahrb ü cher. Abteilung f ü r Sys- He , J. L. , E. P. Ma , Y. C. Shen , W. L. Chen and X. Q. Sun . 1994 . tematik und Ö kologie der Tiere 117 : 401 – 439 . Observations of the biological characteristics of Harmonia Hon eˇ k , A. , A. F. G. Dixon and Z. Martinkov á . 2008 . axyridis (Pallas) (Coleoptera: Coccinellidae). J. Shanghai Body size, reproductive allocation, and maximum repro- Agric. Coll. 12 : 119 – 124 . ductive rate of two species of aphidophagous Coccinellidae Hemptinne , J. L. , A. F. G. Dixon and J. Coffi n . 1992 . Attack exploiting the same resource. Entomol. Exp. Appl. 127 : strategy of ladybird beetles (Coccinellidae): factors shaping 1 – 9 . their numerical response. Oecologia 90 : 238 – 245 . Hon eˇ k , A. , Z. Martinkov á and S. Pekar . 2005 . Temporal stabil- Hemptinne , J. L. , G. Lognay and A. F. G. Dixon . 1998 . Mate ity of morph frequency in central European populations of recognition in the two spot ladybird beetle, Adalia bipunc- Adalia bipunctata and A. decempunctata (Coleoptera: Coc- tata: role of chemical and behavioural cues. J. Insect Physiol. cinellidae) . Eur. J. Entomol. 102 : 437 – 442 . 44 : 1163 – 1171 . Hong , O. K. and Y. C. Park . 1996 . Laboratory rearing of the Hemptinne , J. L. , G. Lognay , C. Gauthier and A. F. G. Dixon . aphidophagous ladybeetle, Harmonia axyridis ; yolk protein 2000 . Role of surface chemical signals in egg cannibalism production and fecundity of the summer adult female . and intraguild predation in ladybirds (Coleoptera: Coccinel- Korean J. Appl. Entomol. 35 : 146 – 152 . lidae) . Chemoecology 10 : 123 – 128 . Huang , Z. , S. Ren and P. D. Musa . 2008 . Effects of temperature Hemptinne , J. L., A. F. G. Dixon and B. Adam . 2001 . Do males on development, survival, longevity, and fecundity of the and females of the two- spot ladybird, Adalia bipunctata (L.), Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) preda- differ in when they mature sexually? J. Insect Behav. 14 : tor, Axinoscymnus cardilobus (Coleoptera: Coccinellidae) . 411 – 419 . Biol. Contr. 46 : 209 – 215 . Life history and development 101
Hukushima , S. and S. Kouyama . 1974 . Life histories and food 2 - spot ladybird, Adalia bipunctata (Coleoptera, Coccinelli- habits of Menochilus sexmaculatus Fabricius (Coleoptera: dae) . Heredity 70 , 172 – 178 . Coccinellidae) . Res. Bull. Fac. Agric. Gifu Univ. 36 : 19 – 29 . Kajita , Y. , E. W. Evans and H. Yasuda . 2009 . Reproductive Hukushima , S. and M. Kamei . 1970 . Effects of various species responses of invasive and native predatory lady beetles of aphids as food on development, fecundity and longevity (Coleoptera: Coccinellidae) to varying prey availability . of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Res. Environ. Entomol. 38 : 1283 – 1292 . Bull. Fac. Agric. Gifu Univ. 29 : 53 – 66 . Kajita , Y. and E. W. Evans . 2010 . Alfalfa fi elds promote high Hurst , G. D. D. , F. K. McMeechan and M. E. N. Majerus . 1998 . reproductive rate of an invasive predatory lady beetle . Biol. Phoridae (Diptera) parasitizing Coccinella septempunctata Invasions 12 : 2293 – 2302 . (Coleoptera: Coccinellidae) select older prepupal hosts . Eur. Kalushkov , P. 1998 . Ten aphid species (Sternorrhyncha: J. Entomol. 95 : 179 – 181 . Aphididae) as prey for Adalia bipunctata (Coleoptera: Coc- Iablokoff - Khnzorian , S. M. 1982 . Les Coccinelles. Soci é t é Nou- cinellidae) . Eur. J. Entomol. 95 : 343 – 349 . velle des É ditions Boub é e , Paris . 568 pp. Kalushkov , P. and I. Hodek . 2004 . The effects of thirteen Ibrahim , M. M. 1955 . Studies on Coccinella undecimpunctata species of aphids on some life history parameters of the aegyptiaca Reiche. 2. Biology and life history . Bull. Soc. ladybird Coccinella septempunctata . BioControl 49 : 21 – Entomol. Egypte 39 : 395 – 423 . 32 . Isikber , A. A. and M. J. W. Copland . 2001 . Food consumption Kalushkov , P. and I. Hodek . 2005 . The effects of six species of and utilisation by larvae of two coccinellid predators, aphids on some life history parameters of the ladybird Pro- Scymnus levaillanti and Cycloneda sanguinea , on cotton pylea quatuordecimpunctata (Coleoptera: Coccinellidae). Eur. aphid, Aphis gossypii . BioControl 46 : 455 – 467 . J. Entomol. 102 : 449 – 452 . Iwata , K. 1932 . On the biology of two large lady - birds in Kalushkov , P. and O. Nedv eˇ d . 2005 . Genetically modifi ed pota- Japan . Trans. Kansai Ent. Soc. 3 : 13 – 26 . toes expressing Cry 3A protein do not affect aphidophagous Izhevsky , S. S. and A. D. Orlinsky . 1988 . Life history of the coccinellids . J. Appl. Entomol. 129 : 401 – 406 . imported Scymnus (Nephus) reunioni (Col.: Coccinellidae) Kalushkov , P. K. 1994 . Longevity, fecundity and development predator of mealybugs. Entomophaga 33 : 101 – 114 . of Adalia bipunctata (L.) (Col., Coccinellidae) when reared on Jalali , M. A. , L. Tirry , A. Arbab and P . De Clercq . 2010 . three aphid diets . Anz. Schad. Pfl sch. Umweltschutz 67 : Temperature - dependent development of the two - spotted 6 – 7 . ladybeetle, Adalia bipunctata , on the green peach aphid, Kaneko , S. , A. Ozawa , T. Saito , A. Tatara , H. Katayama and Myzus persicae, and a factitious food under constant tem- M. Doi . 2006 . Relationship between the seasonal preva- peratures . J. Insect Sci. 10 : article 124 . lence of the predacious coccinellid Pseudoscymnus hareja Jalali , M. A. , L. Tirry and P . De Clercq . 2009a . Effects of food (Coleoptera: Coccinellidae) and the mulberry scale Pseu- and temperature on development, fecundity and life - table daulacaspis pentagona (Hemiptera: Diaspididae) in tea fi elds: parameters of Adalia bipunctata (Coleoptera: Coccinellidae). Monitoring using sticky traps. Appl. Entomol. Zool. 41 : J. Appl. Entomol. 133 : 615 – 625 . 621 – 626 . Jalali , M. A. , L. Tirry and P. De Clercq . 2009b . Food consump- Kanervo , V. 1946 . Studien ü ber die nat ü rlichen Feinde des tion and immature growth of Adalia bipunctata (Coleoptera: Erlenblattk ä fers, Melasoma aenea L. (Col., Crysomelidae). Coccinellidae) on a natural prey and a factitious food. Eur. Annals Zool. Soc. Vanamo 12 : 206 pp. (In Finnish with J. Entomol. 106 : 193 – 198 . German summary.) Jalali , S. K. and S. P. Singh . 1989 . Biotic potential of three Katakura , H. 1976 . On the life cycle of Epilachna admirabilis coccinellid predators on various diaspine hosts . J. Biol. (Coleoptera, Coccinellidae) in Sapporo, northern Japan, Control 3 : 20 – 23 . with special reference to its hibernation by adult stage. Jarosik , V. , A. Hon eˇ k and A. F. G. Dixon . 2002 . Developmental Kontyu 44 : 334 – 336 . rate isomorphy in insects and mites . Am. Nat. 160 : Katsarou , I. , J. T. Margaritopoulos , J. A. Tsitsipis , D. C. 497 – 510 . Perdikis and K. D. Zarpas . 2005 . Effect of temperature de Jong , P. W. , S. W. S. Gessekloo and P. M. Brakefi eld . 1996 . on development, growth and feeding of Coccinella sep- Differences in thermal balance, body temperature and tempunctata and Hippodamia converg ens reared on the activity between non- melanic and melanic two- spot lady- tobacco aphid, Myzus persicae nicotianae . BioControl 50 : bird beetles (Adalia bipunctata ) under controlled conditions . 565 – 580 . J. Exp. Biol. 199 : 2655 – 2666 . Katsoyannos , P. , D. C. Kontodimas and G. J. Stathas . 1997 . de Jong , P. W. , P. M. Brakefi eld and B. P. Geerinck . 1998 . The Phenology of Hippodamia undecimnotata (Col.: Coccinelli- effect of female mating history on sperm precedence in the dae) in Greece. Entomophaga 42 : BP 283 – 293 . two - spot ladybird, Adalia bipunctata (Coleoptera, Coccinel- Kawauchi , S. 1981 . The number of oviposition, hatchability lidae) . Behavioral Ecology 9 : 559 – 565 . and the term of oviposition of Propylea japonica Thunberg de Jong , P. W. , M. D. Verhoog and P. M. Brakefi eld . 1993 . (Coleoptera, Coccinellidae) under different food condition. Sperm competition and melanic polymorphism in the Kontyu 49 : 183 – 191 . 102 O. Nedveˇ d and A. Honeˇk
Kawauchi , S. 1985 . Comparative studies on the fecundity of V - nigrum Muls. (Coleoptera, Coccinellidae) en vue de son three aphidophagous coccinellids (Coleoptera: Coccinelli- introduction en France . 109 Congr. Nat. Soc. Savantes Dijon dae) . Japan. J. Appl. Entomol. Zool. 29 : 203 – 209 . 2 : 275 – 282 . Kesten , U. 1969 . Zur Morphologie und Biologie von Anatis Kutuk , H. and A. Yigit . 2007 . Life table of Delphastus catalinae ocellata (L) (Coleoptera: Coccinellidae) . Z. Angew. Entomol. (Horn) (Coleoptera: Coccinellidae) on cotton whitefl y, 63 : 412 – 445 . Bemisia tabaci (Genn. ) (Homoptera: Aleyrodidae) as prey . Kim , G. H. and S. Y. Choi . 1985 . Effects of the composition of J. Plant Dis. Prot. 114 : 20 – 25 . artifi cial diets on the growth and ovarian development of Kuznetsov , V. N. 1975 . Fauna and ecology of Coccinellidae of an aphidivorous coccinellid beetle ( Harmonia axyridis Ussuri . Trudy Inst. Biopedol. 28 : 3 – 24 . (In Russian.) Pallas: Coccinellidae, Coleoptera). Korean J. Entomol. 15 : Labrie , G. , E. Lucas and D. Coderre . 2006 . Can developmental 33 – 41 . and behavioral characteristics of the multicolored Asian Kingsolver , J. G. and R. B. Huey . 2008 . Size, temperature, and lady beetle Harmonia axyridis explain its invasive success? fi tness: three rules . Evol. Ecol. Res. 10 : 251 – 268 . Biol. Invasions 8 : 743 – 754 . Kishimoto , H. 2003 . Development and oviposition of preda- Lactin , D. J. , N. J. Holliday , D. L. Johnson and R. Craigen . 1995 . cious insects, Stethorus japonicus (Coleoptera: Coccinelli- Improved rate model of temperature- dependent develop- dae), Oligota kashmirica benefi ca (Coleoptera: Staphylinidae), ment by arthropods. Env. Entomol. 24 : 68 – 75 . and Scolothrips takahashii (Thysanoptera: Thripidae) reared LaMana , M. L. and J. C. Miller . 1995 . Temperature - dependent on different spider mite species (Acari: Tetranychidae) . development in a polymorphic lady beetle, Calvia quatuor- Appl. Entomol. Zool. 38 : 15 – 21 . decimguttata (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Klausnitzer , B. 1969a . Zur Kenntnis der Larve von Lithophilus Am. 88 : 785 – 790 . connatus (PANZER) (Col., Coccinellidae). Entomol. Nachrich- LaMana , M. L. and J. C. Miller . 1998 . Temperature - dependent ten 13 : 33 – 36 . development in an Oregon population of Harmonia axyridis Klausnitzer , B. 1969b . Zur Unterscheidung der Eier mitteleu- (Coleoptera: Coccinellidae) . Env. Entomol. 27 : 1001 – rop ä ischer Coccinellidae. Acta Entomol . Bohemoslov. 66 : 1005 . 146 – 149 . Lanzoni , A. , G. Accinelli , G. G. Bazzocchi and G. Burgio . Klausnitzer , B. and H. Klausnitzer . 1986 . Marienk ä fer (Coc- 2004 . Biological traits and life table of the exotic Harmonia cinellidae). A. Ziemsen Verlag, Wittenberg, Lutherstadt . axyridis compared with Hippodamia variegata , and Adalia 104 pp. bipunctata (Col.: Coccinellidae) . J. Appl. Entomol. 128 : Koch , R. L., M. A. Carrillo , R. C. Venette , C. A. Cannon and W. 298 – 306 . D. Hutchison . 2004 . Cold hardiness of the multicolored Li , Y. H. and J. Romeis . 2010 . Bt maize expressing Cry3Bb1 Asian lady beetle (Coleoptera: Coccinellidae). Environ. does not harm the spider mite, Tetranychus urticae, or its Entomol. 33 : 815 – 822 . ladybird beetle predator, Stethorus punctillum . Biol. Control Kontodimas , D. C. and G. J. Stathas . 2005 . Phenology, fecun- 53 : 337 – 344 . dity and life table parameters of the predator Hippodamia Liere , H. and I. Perfect . 2008 . Cheating on a mutualism: Indi- variegata reared on Dysaphis crataegi . BioControl 50 : rect benefi ts of ant attendance to a coccidophagous coc- 223 – 233 . cinellid . Environ. Entomol. 37 : 143 – 149 . Kontodimas , D. C. , P. A. Eliopoulos , G. J. Stathas and L. P. Liu , C. Y. 1933 . Notes on the biology of two giant coccinellids Economou . 2004 . Comparative temperature - dependent in Kwangsi ( Caria dilatata Fabr. and Synonycha grandis development of Nephus includens (Kirsch) and Nephus bisig- Thunb.) with special reference to the morphology of natus (Boehman) (Coleoptera: Coccinellidae) preying on Caria dilatata . Year Book Bur. Entomol., Hangchow 1 : Planococcus citri (Risso) (Homoptera: Psudococcidae): eval- 205 – 250 . uation of a linear and various nonlinear models using spe- Liu , T. X. and P. A. Stansly . 1996a . Morphology of Nephaspis cifi c criteria. Env. Entomol. 33 : 1 – 11 . oculatus and Delphastus pusillus (Coleoptera: Coccinellidae), Kontodimas , D. C. , P. G. Milonas , G. J. Stathas , L. P. Economou predators of Bemisia argentifolii (Homoptera: Aleyrodidae) . and N. G. Kavallieratos . 2007 . Life table parameters of the Proc. Entomol. Soc. Wash. 98 : 292 – 300 . pseudococcid predators Nephus includens and Nephus bisig- Liu , T. X. , P. A. Stansly , K. A. Hoelmer and L. S. Osborne . 1997 . natus (Coleoptera: Coccinellidae) . Eur. J. Entomol. 104 : Life history of Nephaspis oculatus (Coleoptera: Coccinelli- 407 – 415 . dae), a predator of Bemisia argentifolii (Homoptera: Aleyro- Kreiter , S. 1985 . É tude bio é cologique d ’Olla v - nigrum (Mulsant) didae) . Ann. Entomo. Soc. Am. 90 : 776 – 782 . et essai de quantifi cation de l ’ é fi cacit é predatrice d ’Adalia Lombaert , E. , T. Malausa , R. Devred and A. Estoup . 2008 . bipunctata (L.) contre les aphides en verger de pê chers (Cole- Phenotypic variation in invasive and biocontrol popula- optera, Coccinellidae) . Th é se : Universit é de Droit, d ’ É conomie tions of the harlequin ladybird, Harmonia axyridis . BioCon- et des Sciences d ’ Aix - Marseille . 326 pp. trol 53 : 89 – 102 . Kreiter , S. and G. Iperti . 1984 . É tude des potentialit é s Lommen , S. T. E. , P. W. De Jong and P. M. Brakefi eld . 2005 . biologiques et é cologiques d ’ un pr é dateur aphidiphage Olla Phenotypic plasticity of elytron length in wingless two - spot Life history and development 103
ladybird beetles, Adalia bipunctata (Coleoptera: Coceinelli- Matsucoccus resinosae Bean and Godwin (Homoptera: Mar- dae) . Eur. J. Entomol. 102 : 553 – 556 . garodidae) in the United States. Environ. Entomol. 16 : Lommen , S. T. E. , C. W. Middendorp , C. A. Luijten et al. 2008 . 224 – 230 . Natural fl ightless morphs of the ladybird beetle Adalia McKenzie , H. L. 1932 . The biology and feeding habits of bipunctata improve biological control of aphids on single Hyperaspis lateralis Mulsant . Calif. Univ. Pubs. Ent. 6 : plants . Biol. Control 47 : 340 – 346 . 9 – 20 . Lu , W. H. and M. E. Montgomery . 2001 . Oviposition, develop- McMullen , R. D. 1967 . The effects of photoperiod, tempera- ment, and feeding of Scymnus ( Neopullus ) sinuanodulus ture and food supply on rate of development and diapause (Coleoptera: Coccinellidae): a predator of Adelges tsugae in Coccinella novemnotata . Can. Entomol. 99 : 578 – 586 . (Homoptera: Adelgidae) . Ann. Entomol. Soc. Am. 94 : M ’ Hamed , T. B. and M. Chemseddine . 2001 . Assessment of 64 – 70 . temperature effects on the development and fecundity of Lu , W. H. , P. Souphanya and M. E. Montgomery . 2002 . Pullus mediterraneus (Col. , Coccinellidae) and consumption Descriptions of immature stages of Scymnus (Neopullus ) of Saissetia oleae eggs (Hom. , Coccoida) . J. Appl. Entomol. sinuanodulus Yu and Yao (Coleoptera: Coccinellidae) with 125 : 527 – 531 . notes on life history. Col. Bull. 56 : 127 – 141 . Mishra , G. and Omkar . 2004 . Diel rhythmicity of certain life Lucas , E. , D. Coderre and J. Brodeur . 2000 . Selection of events of a ladybird, Propylea dissecta (Mulsant) . Biol. molting and pupation sites by Coleomegilla maculata (Cole- Rhythm Res. 35 : 269 – 276 . optera: Coccinellidae): avoidance of intraguild predation. Mishra , G. and Omkar . 2006 . Conspecifi c interference by Environ. Entomol. 29 : 454 – 459 . adults in an aphidophagous ladybird Propylea dissecta (Cole- Lusis , Ya. Ya . 1961 . On the biological meaning of colour poly- optera: Coccinellidae): effect on reproduction . Bull. Entomol. morphism of lady- beetle Adalia bipunctata L . Latv. Entomol. Res. 96 : 407 – 412 . 4 : 2 – 29 . (In Russian with English summary.) Mori , K. , M. Nozawa , K. Arai and T. Gotoh . 2005 . Life - Lundgren , J. G. and R. N. Wiedenmann . 2002 . Coleopteran - history traits of the acarophagous lady beetle, Stethorus specifi c Cry3Bb toxin from transgenic corn pollen does not japonicus at three constant temperatures . BioControl 50 : affect the fi tness of a nontarget species, Coleomegilla macu- 35 – 51 . lata DeGeer (Coleoptera: Coccinellidae) . Environ. Entomol. Mota , J. A. , A. O. Soares and P. V. Garcia . 2008 . Temperature 31 : 1213 – 1218 . dependence for development of the whitefl y predator Clito- Lundgren , J. G. , L. S. Hesler , K. Tilmon , K. Dashiell and R. stethus arcuatus (Rossi) . BioControl 53 : 603 – 613 . Scott . 2009 . Direct effects of soybean varietal selection and Muggleton , J. 1979 . Non - random mating in wild populations Aphis glycines- resistant soybeans on natural enemies. of polymorphic Adalia bipunctata . Heredity 42 : 57 – 65 . Arthropod - Plant Interactions 3 : 9 – 16 . Muralidharan , C. M. 1994 . Biology and feeding potential of Majerus , M. E. N. 1994 . Ladybirds. Harper Collins Publishers, black beetle (Chilocorus nigritus ), a predator on date palm London . 367 pp. scale (Parlatoria blanchardii ) . Indian J. Agric. Sci. 64 : Majerus , M. E. N. 1997 . Interspecifi c hybridisation in lady- 270 – 271 . birds (Col.: Coccinellidae) . Entomologist ’ s Record 109 : Nakanishi , K. , M. Hoshino , M. Nakai and Y. Kunimi . 2008 . 11 – 23 . Novel RNA sequences associated with late male killing in Majerus , M. E. N. 1998 . Melanism. Evolution in action . Oxford Homona magnanima . Proc. Royal Soc. B - Biol. Sci. 275 : University Press, Oxford , 338 pp. 1249 – 1254 . Majerus , M. E. N. , P. O ’ Donald and J. Weir . 1982a . Evidence Nakano , S. and H. Katakura . 1999 . Morphology and biology for preferential mating in Adalia bipunctata . Heredity 49 : of a phytophagous ladybird beetle, Epilachna pusillanima 37 – 49 . (Coleoptera: Coccinellidae) newly recorded on Ishigaki Majerus , M. E. N. , P. O ’ Donald and J. Weir . 1982b . Female Island, the Ryukyus. Appl. Entomol. Zool. 34 : 189 – 194 . mating preference is genetic. Nature (London) 300 : Nalepa , C. A. , K. A. Kidd and K. R. Ahlstrom . 1996 . Biology 521 – 523 . of Harmonia axyridis (Coleoptera: Coccinellidae) in winter Majerus , M. E. N. and I. A. Zakcharov . 2000 . Does thermal aggregations . Ann. Entomol. Soc. Am. 89 : 681 – 685 . melanism maintain melanic polymorphism in the two - spot Nalepa , C. A. and A. Weir . 2007 . Infection of Harmonia ladybird Adalia bipunctata (Coleoptera: Coccinellidae)? axyridis (Coleoptera: Coccinellidae) by Hesperomyces vires- Zhurnal Obshchei Biologii 61 : 381 – 392 . cens (Ascomycetes: Laboulbeniales): role of mating status Matsubayashi , K. W. and H. Katakura . 2007 . Unilateral and aggregation behavior. J. Invertebrate Pathol. 94 : mate choice causes bilateral behavioral isolation between 196 – 203 . two closely related phytophagous ladybird beetles Naranjo , S. E. , R. L. Gibson and D. D. Walgenbach . 1990 . (Coleoptera: Coccinellidae: Epilachninae) . Ethol. 113 : 686 – Development, survival, and reproduction of Scymnus fron- 691 . talis (Coleoptera: Coccinellidae), an imported predator of McClure , M. S. 1987 . Potential of the Asian predator, Harmo- Russian wheat aphid, at four fl uctuating temperatures . nia axyridis Pallas (Coleoptera: Coccinellidae), to control Ann. Entomol. Soc. Am. 83 : 527 – 531 . 104 O. Nedveˇ d and A. Honeˇk
N e d v eˇ d , O. 1994 . Cold Hardiness of Ladybirds (Chladov á odol- cinella septempunctata (Coleoptera: Coccinellidae) from four nost slun é cˇ ek.) PhD thesis, Institute of Entomology, Cˇ esk é latitudes in Japan. Appl. Entomol. Zool. 32 : 567 – 572 . Bud eˇjovice. 116 pp. (In Czech.) Oliver , T. H. , I. Jones , J. M. Cook and S. R. Leather . 2008 . N e d v eˇ d , O. and I. Hodek . 1995 . Confi nement stimulates trivial Avoidance responses of an aphidophagous ladybird, Adalia fl ight in Coccinella septempunctata (Coleoptera: Coccinelli- bipunctata , to aphid - tending ants . Ecol. Entomol. 33 : dae) . Eur. J. Entomol. 92 : 719 – 722 . 523 – 528 . Ng , S. M. 1986 . Egg mortality of four species of aphidopha- Olszak , R. W. 1987 . The occurrence of Adalia bipunctata (L. ) gous Coccinellidae in Malaysia . In I. Hodek (ed). Ecology of (Coleoptera, Coccinellidae) in apple orchards and the effect Aphidophaga . Academia , Prague . pp 77 – 81 . of different factors on its development. Ekol. Polska 35 : Ng , S. M. 1988 . Observations on the foraging behaviour of 755 – 765 . starved aphidophagous coccinellid larvae (Coleoptera: Coc- Omkar and G. Mishra . 2005a . Evolutionary signifi cance of cinellidae ). In E. Niemczyk and A. F. G. Dixon (eds). Ecology promiscuity in an aphidophagous ladybird, Propylea dis- and Effectiveness of Aphidophaga . SPB Acad. Publ. , The secta (Coleoptera: Coccinellidae). Bull. Entomol. Res. 95 : Hague . pp. 199 – 206 . 527 – 533 . Ng , S. M. 1991 . Voracity, development and growth of larvae Omkar and G. Mishra . 2005b . Mating in aphidophagous lady- of Menochilus sexmaculatus (Coleoptera: Coccinellidae) fed birds: costs and benefi ts . J. Appl. Entomol. 129 : 432 – 436 . on Aphis spiraecola . In L. Polg á r , R. J. Chambers , A. F. G. Omkar and S. Pathak . 2006 . Effects of different photoperiods Dixon and I. Hodek (eds). Behaviour and Impact of Aphido- and wavelengths of light on the life- history traits of an phaga . SPB Acad. Publ. , The Hague . pp. 199 – 206 . aphidophagous ladybird, Coelophora saucia (Mulsant) . J. Obata , S. 1988 . Mating behaviour and sperm transfer in the Appl. Entomol. 130 : 45 – 50 . ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coc- Omkar and S. Pathak . 2009 . Crowding affects the life cinellidae) . In E. Niemczyk and A. F. G. Dixon (eds). Ecology attributes of an aphidophagous ladybird beetle, Propylea and Effectiveness of Aphidophaga . SPB Acad. Publ. , The dissecta . Bull. Insectology 62 : 35 – 40 . Hague . pp. 39 – 42 . Omkar and A. Pervez . 2002 . Infl uence of temperature on Obata , S. and T. Hidaka . 1987 . Ejection and ingestion of the age - specifi c fecundity of the ladybeetle Micraspis discolor spermatophore by the female ladybird beetle, Harmonia (Fabricius) . Insect Sci. Appl. 22 : 61 – 65 . axyridis Pallas (Coleoptera: Coccinellidae) . Can. Entomol. Omkar and A. Pervez . 2003 . Ecology and biocontrol potential 119 : 603 – 604 . of a scale - predator, Chilocorus nigritus . Biocontrol Sci. Obrycki , J. J. and M. J. Tauber . 1981 . Phenology of three coc- Technol. 13 : 379 – 390 . cinellid species: thermal requirements for development . Omkar and A. Pervez . 2004a . Comparative demographics of Ann. Entomol. Soc. Am. 74 : 31 – 36 . a generalist predatory ladybird on fi ve aphid prey: a labora- Obrycki , J. J. , K. L. Giles and A. M. Ormord . 1998 . Interactions tory study. Insect Sci. 11 : 211 – 218 . between an introduced and indigenous coccinellid species Omkar and A. Pervez . 2004b . Temperature - dependent devel- at different prey densities. Oecologia 117 : 279 – 285 . opment and immature survival of an aphidophagous lady- O ’ Donald , P. and M. E. N. Majerus . 1989 . Sexual selection beetle, Propylea dissecta (Mulsant) . J. Appl. Entomol. 128 : models and the evolution of melanism in ladybirds . In 510 – 514 . F. M. W. Feldman (ed). Mathematical Evolutionary Theory . Omkar and A. Pervez . 2005 . Mating behavior of an aphido- Princeton University Press , Princeton, NJ . pp. 247 – 269 . phagous ladybird beetle, Propylea dissecta (Mulsant) . Insect Ohashi , K. , Y. Sakuratani , N. Osawa , S. Yano and A. Takafuji . Sci. 12 : 37 – 44 . 2005 . Thermal microhabitat use by the ladybird beetle, Omkar and S. K. Singh . 2007 . Rhythmicity in life events of Coccinella septempunctata (Coleoptera: Coccinellidae), and an aphidophagous ladybird beetle, Cheilomenes sexmaculata . its life cycle consequences . Environ. Entomol. 34 : J. Appl. Entomol. 131 : 85 – 89 . 432 – 439 . Omkar and S. Srivastava . 2003 . Infl uence of six aphid prey Okrouhla , M. , S. Chakrabarti and I. Hodek . 1983 . Develop- species on development and reproduction of a ladybird mental rate and feeding capacity in Cheilomenes sulphurea beetle, Coccinella septempunctata . BioControl 48 : 379 – 393 . (Coleoptera: Coccinellidae) . V eˇ st. C ˇ s. Spole cˇ . Zool. 47 : Omkar , G. Kumar and J. Sahu . 2009 . Performance of a preda- 105 – 117 . tory ladybird beetle, Anegleis cardoni (Coleoptera: Coccinel- Okuda , T. , M. Hodkov á and I. Hodek . 1986 . Flight tendency lidae) on three aphid species. Eur. J. Entomol. 106 : in Coccinella septempunctata in relation to changes in fl ight 565 – 572 . muscles, ovaries and corpus allatum. In I. Hodek (ed.). Omkar , G. Mishra , S. Srivastava and A. K. Gupta . 2004 . Ovi- Ecology of Aphidophaga. Academia, Prague, W. Junk, Dor- positional rhythmicity in ladybirds (Coleoptera: Coccinelli- drecht . pp. 217 – 223 . dae): a laboratory study. Biol. Rhythm Res. 35 : 277 – 287 . Okuda , T. , T. Gomi and I. Hodek . 1997 . Effect of temperature Omkar , G. Mishra , S. Srivastava , A. K. Gupta and S. K. Singh . on pupal pigmentation and size of the elytral spots in Coc- 2005a . Reproductive performance of four aphidophagous Life history and development 105
ladybirds on cowpea aphid, Aphis craccivora Koch . J. Appl. Perumalsamy , K. , R. Selvasundaram , A. Roobakkumar , V. J. Entomol. 129 : 217 – 220 . Rahman and N. Muraleedharan . 2010 . Life table and pred- Omkar , A. Pervez , G. Mishra , S. Srivastava , S. K. Singh and A. atory effi ciency of Stethorus gilvifrons (Coleoptera: Coccinel- K. Gupta . 2005b . Intrinsic advantages of Cheilomenes sex- lidae), an important predator of the red spider mite, maculata over two coexisting Coccinella species (Coleoptera: Oligonychus coffeae (Acari: Tetranychidae), infesting tea . Coccinellidae) . Insect Sci. 12 : 179 – 184 . Exp. Appl. Acarol. 50 : 141 – 150 . Omkar , S. K. Singh and G. Mishra . 2010a . Multiple matings Pervez , A. , Omkar and A. S. Richmond . 2004 . The infl uence affect the reproductive performance of the aphidophagous of age on reproductive performance of the predatory lady- ladybird beetle, Coelophora saucia (Coleoptera: Coccinelli- bird beetle, Propylea dissecta . J. Insect Sci. 4 : 22 . dae) . Eur. J. Entomol. 107 : 177 – 182 . Phoofolo , M. W. , J. J. Obrycki and E. S. Krafsur . 1995 . Omkar , S. K. Singh and G. Mishra . 2010b . Parental age at Temperature - dependent ovarian development in Coccinella mating affects reproductive attributes of the aphidopha- septempunctata (Coleoptera, Coccinellidae) . Ann. Entomol. gous ladybird beetle, Coelophora saucia (Coleoptera: Coc- Soc. Am. 88 : 72 – 79 . cinellidae) . Eur. J. Entomol. 107 : 341 – 347 . Phoofolo , M. W. , K. L. Giles and N. C. Elliott . 2007 . Quantita- Omkar , K. Singh and A. Pervez . 2006a . Infl uence of mating tive evaluation of suitability of the greenbug, Schizaphis duration on fecundity and fertility in two aphidophagous graminum, and the bird cherry- oat aphid, Rhopalosiphum ladybirds . J. Appl. Entomol. 130 : 103 – 107 . padi , as prey for Hippodamia convergens (Coleoptera: Coc- Omkar , S. K. Singh and K. Singh . 2006b . Effect of age on cinellidae) . Biol. Control 41 : 25 – 32 . reproductive attributes of an aphidophagous ladybird, Pilorget , L. , J. Buckner and J. G. Lundgren . 2010 . Sterol limi- Cheilomenes sexmaculata . Insect Sci. 13 : 301 – 308 . tation in a pollen- fed omnivorous lady beetle (Coleoptera: Orivel , J. , P. Servigne , P. Cerdan , A. Dejean and B. Corbara . Coccinellidae) . J. Insect Physiol. 56 : 81 – 87 . 2004 . The ladybird Thalassa saginata, an obligatory Ponsonby , D. J. 2009 . Factors affecting utility of Chilocorus myrmecophile of Dolichoderus bidens ant colonies . Natur- nigritus (F.) (Coleoptera: Coccinellidae) as a biocontrol wissenschaften 91 : 97 – 100 . agent . CAB Reviews: Perspectives in Agriculture, Veterinary Omkar and S. Srivastava . 2002 . The reproductive behaviour Science, Nutrition and Natural Resources 4 : 1 – 20 . of an aphidophagous ladybeetle, Coccinella septempunctata Ponsonby , D. J. and M. J. W. Copland . 1996 . Effect of tempera- Linnaeus . Eur. J. Entomol. 99 : 465 – 470 . ture on development and immature survival in the scale Osawa , N. 1994 . The occurrence of multiple mating in a wild insect predator, Chilocorus nigritus (F.) (Coleoptera: Coc- population of a ladybird beetle Harmonia axyridis Pallas cinellidae) . Biocontrol Sci. Technol. 6 : 101 – 109 . (Coleoptera: Coccinellidae) . J. Ethol. 12 : 63 – 66 . Ponsonby , D. J. and M. J. W. Copland . 1998 . Environmental Osawa , N. 2005 . The effect of prey availability on ovarian infl uences on fecundity, egg viability and egg cannibalism development and oosorption in the ladybird beetle Harmo- in the scale insect predator, Chilocorus nigritus . BioControl nia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 43 : 39 – 52 . 102 : 503 – 511 . Ponsonby , D. J. and M. J. W. Copland . 2007 . Infl uence of Osawa , N. and T. Nishida . 1992 . Seasonal variation in elytral host density and population structure on egg production colour polymorphism in Harmonia axyridis (the ladybird in the coccidophagous ladybird, Chilocorus nigritus F. beetle): the role of non - random mating . Heredity 69 : (Coleoptera: Coccinellidae). Agric. Forest Entomol. 9 : 297 – 307 . 287 – 296 . Osawa , N. and K. Ohashi . 2008 . Sympatric coexistence of Poprawski , T. J. , J. C. Legaspi and P. E. Parker . 1998 . Infl uence sibling species Harmonia yedoensis and H. axyridis (Coleop- of entomopathogenic fungi on Serangium parcesetosum tera: Coccinellidae) and the roles of maternal investment (Coleoptera: Coccinellidae), an important predator of through egg and sibling cannibalism. Eur. J. Entomol. 105 : whitefl ies (Homoptera: Aleyrodidae). Environ. Entomol. 27 : 445 – 454 . 785 – 795 . Pantyukhov , G. A. 1968 . A study of ecology and physiology Prevolsek , J. and T. D. Williams . 2006 . Individual variation of the predatory beetle Chilocorus rubidus Hope (Coleoptera, and plasticity in egg size in multicolored Asian lady beetles Coccinellidae) . Zool. Zh. 47 : 376 – 386 . (In Russian with (Harmonia axyridis ) . Integr. Comp. Biol. 46 Suppl. 1 : E238 – English summary.) E238 (abstract). Perry , J. C. and B. D. Roitberg . 2005 . Ladybird mothers miti- Putman , W. L. 1955 . Bionomics of Stethorus punctillum Weise gate offspring starvation risk by laying trophic eggs. Behav. in Ontario. Can. Entomol. 87 : 9 – 33 . Ecol. Sociobiol. 58 : 578 – 586 . Radwan , Z. and G. L. Lovei . 1983 . Aphids as prey for the coc- Perry , J. C. , D. M. T. Sharpe and L. Rowe . 2009 . Condition - cinellid Exochomus quadripustulatus . Entomol. Exp. Appl. 34 : dependent female remating resistance generates sexual 283 – 286 . selection on male size in a ladybird beetle. Anim. Behav. 77 : Rana , J. S. and J. Kakker . 2000 . Biological studies on 7 - spot 743 – 748 . ladybird beetle, Coccinella septempunctata L. with cereal 106 O. Nedveˇ d and A. Honeˇk
aphid, Sitobion avenae (F.) as prey . Cereal Res. Comm. 28 : Roy , H. E. , H. Rudge , L. Goldrick and D. Hawkins . 2007 . Eat 449 – 454 . or be eaten: prevalence and impact of egg cannibalism on Rathour , Y. S. and T. Singh . 1991 . Importance of ovariole two - spot ladybirds, Adalia bipunctata . Entomol. Exp. Appl. number in Coccinellidae (Coleoptera). Entomon 16 : 125 : 33 – 38 . 35 – 41 . Rozsypalova , A. 2007 . Polymorphism in Pupal Colouration in Raworth , D. A. 2001 . Development, larval voracity, and Ladybirds . (Polymorfi zmus zbarven í kukel slun é cˇ ek.) Bach- greenhouse releases of Stethorus punctillum (Coleoptera: elor thesis, University of South Bohemia, C ˇ esk é Bud eˇ jovice. Coccinellidae) . Can. Entomol. 133 : 721 – 724 . 23 pp. (In Czech.) Ren , S. X. , P. A. Stansly and T. X. Liu . 2002 . Life history of the dos Santos , N. R. P. , T. M. dos Santos - Cividanes , F. J. Cividanes , whitefl y predator Nephaspis oculatus (Coleoptera: Coccinelli- A. C. R. dos Anjos and L. V. R. de Oliveira . 2009 . Biological dae) at six constant temperatures. Biol. Contr. 23 : aspects of Harmonia axyridis fed on two prey species and 262 – 268 . intraguild predation with Eriopis connexa . Pesquisa Agro- Rhamhalinghan , M. 1985 . Intraspecifi c variations in ovariole pecuaria Bras. 44 : 554 – 560 . number / ovary in Coccinella septempunctata L. (Coleoptera: dos Santos , T. M. 1992 . Aspectos morphol ó gicos e efeito da tem- Coccinellidae) . Ind. Zool. 9 : 91 – 97 . peratura sobre a biologia de Scymnus ( Pullus) argentinicus Rhamhalinghan , M. 1986 . Seasonal variations in ovariole (Weise, 1906. (Coleoptera: Coccinellidae) alimentados com number/ovary in Coccinella septempunctata L. (Coleoptera: pulg ã o verde Schizaphis graminum (Rondani, 1852. (Homop- Coccinellidae) . Proc. Indian Natn. Sci. Acad. 52 : 619 – 623 . tera: Aphididae) . Thesis, Escola superior de Agricultura de Rhamhalinghan , M. 1999 . Variations in the realized fecun- Lavras, Minas Gerais. 107 pp. dity of melanics of Coccinella septempunctata L. in relation Savoiskaya , G. I. 1965 . Biology and perspectives of utilisation to degree of elytral pigmentation and radiant heat level . of coccinellids in the control of aphids in south - eastern J.of Ins. Sci. 12 : 22 – 26 . Kazakhstan orchards. Trudy Inst. Zashch. Rast., Alma- Ata 9 : Ricci , C. and I. Stella . 1988 . Relationship between morphol- 128 – 156 . (In Russian.) ogy and function in some Palearctic Coccinellidae . In E. Savoiskaya , G. I. 1970 . Coccinellids of the Alma - Ata reserve. Niemczyk and A. F. G. Dixon (eds). Ecology and Effectiveness Trudy Alma - Atin . Gos. Zapov. 9 : 163 – 187 . (In Russian.) of Aphidophaga: Proceedings of an International Symposium, Savoiskaya , G. I. and B. Klausnitzer , 1973 . Morphology and Teresin, Poland, 31 August – 5 September, 1987 . SPB Aca- taxonomy of the larvae with keys for their identifi cation . In demic Publishing , The Hague, The Netherlands . pp. I. Hodek (ed.). Biology of the Coccinellidae . Prague & Hague , 21 – 25 . W. Junk , pp. 36 – 55 . Richards , A. M. and L. W. Filewood . 1988 . The effect of agri- Schade , M. and C. Sengonca . 1998 . On the development, cultural crops and weeds on the bionomics of the pest feeding activity and prey preference of Hippodamia conver- species comprising the Epilachna vigintioctopunctata gens Guer.- Men. (Col., Coccinellidae) preying on Thrips complex (Col., Coccinellidae) . J. Appl.Entomol. 105 : tabaci Lind. (Thys., Thripidae) and two species of Aphidae . 88 – 103 . Anz. Schadlingskunde Pfl anzenschutz Umweltschutz 71 : Rieder , J. P. , T. A. S. Newbold , S. Sato , H. Yasuda and E. W. 77 – 80 . Evans . 2008 . Intra - guild predation and variation in egg Schanderl , H. , A. Ferran and M. M. Larroque . 1985 . Les defence between sympatric and allopatric populations besoins trophiques et thermiques des larves de la coccinelle of two species of ladybird beetles. Ecol. Entomol. 33 : Harmonia axyridis Pallas . Agronomie 5 : 417 – 421 . 53 – 58 . Schanderl , H. , A. Ferran and V. Garcia . 1988 . L ’ é levage de Rodriguez - Saona , C. and J. C. Miller . 1999 . Temperature deux coccinelles Harmonia axyridis et Semiadalia undecimno- dependent effects on development, mortality, and growth tata á l ’ aide d ’ oeufs d ’Anagasta kuehniella tu é s aux rayon of Hippodamia convergens (Coleoptera: Coccinellidae). Env. ultraviolets . Entomol. Exp. Appl. 49 : 235 – 244 . Entomol. 28 : 518 – 522 . Schroder , F. C. , J. J. Farmer , S. R. Smedley , T. Eisner and J. Rossini , C. , A. Gonzalez , J. Farmer , J. Meinwald and T. Eisner . Meinwald . 1998 . Absolute confi guration of the polya- 2000 . Antiinsectan activity of epilachnene, a defensive zamacrolides, macrocyclic polyamines produced by a lady- alkaloid from pupae of Mexican bean beetles (Epilachna var- bird beetle. Tetrahedron Letters 39 : 6625 – 6628 . ivestis ) . J. Chem. Ecol. 26 : 391 – 397 . Schuder , I. , M. Hommes and O. Larink . 2004 . The infl uence Roy , M. , J. Brodeur and C. Cloutier . 2002 . Relationship of temperature on development of Adalia bipunctata (Cole- between temperature and developmental rate of Stethorus optera: Coccinellidae). Eur. J. Entomol. 101 : 379 – 384 . punctillum (Coleoptera: Coccinellidae) and its prey Tetrany- Seko , T. and K. Miura . 2009 . Effects of artifi cial selection for chus mcdanieli (Acarina: Tetranychidae) . Env. Entomol. 31 : reduced fl ight ability on survival rate and fecundity of Har- 177 – 187 . monia axyridis (Pallas) (Coleoptera: Coccinellidae) . Appl. Roy , M. , J. Brodeur and C. Cloutier . 2003 . Effect of tempera- Entomol. Zool. 44 : 587 – 594 . ture on intrinsic rates of natural increase (rm) of a coc- Semyanov , V. P. 1970 . Biological properties of Adalia bipunc- cinellid and its spider mite prey. BioControl 48 : 57 – 72 . tata L. (Coleoptera: Coccinellidae) in conditions of Life history and development 107
Leningrad region . Zashch. Rast. Vredit. Bolez. 127 : 105 – syriacus reared on the green citrus aphid, Aphis spiraecola , 112 . (In Russian.) fed on two host plants. Entomol. Sci. 11 : 281 – 288 . Semyanov , V. P. 1980 . Biology of Calvia quatuordecimguttata L. Srivastava , S. and Omkar . 2003 . Infl uence of temperature on (Coleoptera, Coccinellidae) . Entomol. Obozr. 59 : 757 – 763 . certain biological attributes of a ladybeetle Coccinella sep- (In Russian.) tempunctata Linnaeus . Entomologica Sinica 10 : 185 – 193 . Semyanov , V. P. and E. P. Bereznaya . 1988 . Biology and pros- Srivastava , S. and Omkar . 2004 . Age - specifi c mating and pects of using Vietnam ’ s lady beetle Lemnia biplagiata reproductive senescence in the seven- spotted ladybird, Coc- (Swartz) for control of aphids in greenhouses . In E. Niemc- cinella septempunctata . J. Appl. Entomol. 128 : 452 – 458 . zyk and A. F. G. Dixon (eds), Ecology and Effectiveness of Srivastava , S. and Omkar . 2005 . Mate choice and reproduc- Aphidophaga . SPB Academic , The Hague . pp. 267 – 269 . tive success of two morphs of the seven spotted ladybird, Senal , D. 2006 . Avci b ö cek Chilocorus nigritus (Fabricius) Coccinella septempunctata (Coleoptera: Coccinellidae) . Eur. J. (Coleoptera: Coccinellidae) ’ un bazi biyolojik ve ekolojik ö zellik- Entomol. 102 : 189 – 194 . leri ile dog ˘aya adaptasyonu ü zerinde aras, tirmalar . PhD thesis, Stathas , G. J. 2000 . The effect of temperature on the develop- Department of Plant Protection, Institute of Natural and ment of the predator Rhyzobius lophanthae and its phenol- Applied Sciences, University of Ç ukurova, Turkey. ogy in Greece. BioControl 45 : 439 – 451 . Sengonca , C. and C. Arnold . 2003 . Development, predation Stathas , G. J. , P. A. Eliopoulos , D. C. Kontodimas and J. Gian- and reproduction by Exochomus quadripustulatus L. (Coleop- nopapas . 2001 . Parameters of reproductive activity in tera: Coccinellidae) as predator of Pulvinaria regalis Canard females of Harmonia axyridis (Coleoptera: Coccinellidae). (Homoptera: Coccidae) and its coincidence with the prey in Eur. J. Entomol. 98 : 547 – 549 . the fi eld . J. Plant Dis. Prot. 110 : 250 – 262 . Stathas , G. J. , P. A. Eliopoulos , D. C. Kontodimas and D. T. Seo , M. J. , G. H. Kim and Y. N. Youn . 2008 . Differences in Siamos . 2002 . Adult morphology and life cycle under con- biological and behavioural characteristics of Harmonia stant temperatures of the predator Rhyzobius lophanthae axyridis (Coleoptera: Coccinellidae) according to color Blaisdell (Col., Coccinellidae) . Anz. Sch ä dlingskunde 75 : pattern of elytra. J. Appl. Entomol. 132 : 239 – 247 . 105 – 109 . Shannag , H. K. and W. M. Obeidat . 2008 . Interaction between Stewart , L. A. , A. F. G. Dixon , Z. Ruzicka and G. Iperti . 1991a . plant resistance and predation of Aphis fabae (Homoptera: Clutch and egg size in ladybird beetles. Entomophaga 36 : Aphididae) by Coccinella septempunctata (Coleoptera: Coc- 329 – 333 . cinellidae) . Ann. Appl. Biol. 152 : 331 – 337 . Stewart , L. A. , J. L. Hemptinne and A. F. G. Dixon . 1991b . Simmons , A. M. and J. C. Legaspi . 2004 . Survival and preda- Reproductive tactics of ladybird beetles − relationships tion of Delphastus catalinae (Coleoptera: Coccinellidae), a between egg size, ovariole number and developmental time . predator of whitefl ies (Homoptera: Aleyrodidae), after Func. Ecol. 5 : 380 – 385 . exposure to a range of constant temperatures. Environ. Sugiura , K. and H. Takada . 1998 . Suitability of seven aphid Entomol. 33 : 839 – 843 . species as prey of Cheilomenes sexmaculata (Fabricius) (Cole- Simmons , A. M. , J. C. Legaspi and B. C. Legaspi . 2008 . optera: Coccinellidae) . Japanese J. Appl. Entomol. Zool. 42 : Responses of Delphastus catalinae (Coleoptera: Coccinelli- 7 – 14 . dae), a predator of whitefl ies (Hemiptera: Aleyrodidae), to Sundby , R. A. 1968 . Some factors infl uencing the repro- relative humidity: oviposition, hatch, and immature sur- duction and longevity of Coccinella septempunctata vival . Ann. Entomol. Soc. Am. 101 : 378 – 383 . Linnaeus (Coleoptera: Coccinellidae) . Entomophaga 13 : Sloggett , J. J. 2008 . Weighty matters: body size, diet and spe- 197 – 202 . cialization in aphidophagous ladybird beetles (Coleoptera: Taghizadeh , R. , Y. Fathipour and K. Kamali . 2008 . Infl uence Coccinellidae) . Eur. J. Entomool. 105 : 381 – 389 . of temperature on life - table parameters of Stethorus gilvi- Sloggett , J. J. and M. W. Lorenz . 2008 . Egg composition and frons (Mulsant) (Coleoptera: Coccinellidae) fed on Tetrany- reproductive investment in aphidophagous ladybird beetles chus urticae Koch . J. Appl. Entomol. 132 : 638 – 645 . (Coccinellidae: Coccinellini): egg development and inter- Takahashi , K. 1987 . Differences in oviposition initiation and specifi c variation. Physiol. Entomol. 33 : 200 – 208 . sites of lady beetles, Coccinella septempunctata brucki Mulsant Smedley , S. R. , K. A. Lafl eur , L. K. Gibbons et al. 2002 . Glan- and Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) dular hairs: pupal chemical defense in a non- native lady- in the fi eld . Japanese Journal of Applied Entomology and bird beetle (Coleoptera: Coccinellidae) . Northeastern Nat. 9 : Zoology 31 , 253 – 254 . (In Japanese.) 253 – 266 . Takakura , K. 2004 . Variation in egg size within and among Smith , K. M. , D. Smith and A. T. Lisle . 1999 . Effect of fi eld - generations of the bean weevil, Bruchidius dorsalis (Cole- weathered residues of pyriproxyfen on the predatory coc- optera, Bruchidae): effects of host plant quality and pater- cinellids Chilocorus circumdatus Gyllenhal and Cryptolaemus nal nutritional investment . Ann. Entomol. Soc. Am. 97 : montrouzieri Mulsant . Austr. J. Exp. Agric. 39 : 995 – 1000 . 346 – 352 . Soroushmehr , Z. , A. Sahragard and L. Salehi . 2008 . Com- Takeuchi , M. , A. Shimizu , A. Ishihara and M. Tamura . parative life table statistics for the ladybeetle Scymnus 1999 . Larval diapause induction and termination in a 108 O. Nedveˇ d and A. Honeˇk
phytophagous lady beetle, Epilachna admirabilis Crotch axyridis and the effect of container size. IOBC Bulletin 58 : (Coleoptera: Coccinellidae) . Appl. Entomol. Zool. 34 : 165 – 174 . 475 – 479 . Uygun , N. and R. Atl ı han . 2000 . The effect of temperature on Tanasijevic , N. 1958 . Zur morphologie and biologie des development and fecundity of Scymnus levaillanti . BioCon- luzerne marienk ä fers Subcoccinella vigintiquatuorpunctata L . trol 45 : 453 – 462 . Beitr ä ge zur Entomologie 8 : 23 – 78 . Uygun , N. and N. Z. Elekcioglu . 1998 . Effect of three diaspidi- Tavadjoh , Z. , H. Hamzehzarghani , H. Alemansoor , J. Khal- dae prey species on development and fecundity of the lady- ghani and A. Vikram . 2010 . Biology and feeding behaviour beetle Chilocorus bipustulatus in the laboratory . BioControl of ladybird, Clitostethus arcuatus, the predator of the ash 43 : 153 – 162 . whitefl y, Siphoninus phillyreae, in Fars province, Iran. Waldbauer , G. P. 1964 . The consumption, digestion and J. Insect Sci. 10 : 120 . utilization of solanaceous and non- solanaceous plants T a w fi k , M. F. S. , S. Abul - Nasr and B. M. Saad . 1973 . The by larvae of the tobacco hornworm, Protoparce sexta biology of Scymnus interruptus Goeze (Coleoptera: Coccinel- (Johan) (Lepidoptera: Sphingidae) . Entomol. Exp. Appl. 7 : lidae) . Bull. Soc. Entomol. Egypt 57 : 9 – 26 . 253 – 269 . Thompson , W. R. 1951 . The specifi city of host relations in Wang , S. , J. P. Michaud , R. Z. Zhang , F. Zhang and S. Liu . predaceous insects. Can. Entomol. 1983 : 262 – 269 . 2009 . Seasonal cycles of assortative mating and reproduc- Timms , J. E. L. and S. R. Leather . 2007 . Ladybird egg cluster tive behaviour in polymorphic populations of Harmonia size: relationships between species, oviposition substrate axyridis in China. Ecol. Entomol. 34 : 483 – 494 . and cannibalism. Bull. Entomol. Res. 97 : 613 – 618 . Ware , R. L. and M. E. N. Majerus . 2008 . Intraguild predation Timms , J. E. L. and S. R. Leather . 2008 . How the consumption of immature stages of British and Japanese coccinellids by and development rates of the conifer specialist Aphidecta the invasive ladybird Harmonia axyridis . BioControl 53 : obliterata respond to temperature, and is better adapted to 169 – 188 . limited prey than a generalist? Ann. Appl. Biol. 153 : Ware , R. L. , B. Yguel and M. E. N. Majerus . 2008 . Effects of 63 – 71 . larval diet on female reproductive output of the European Todorova , S. I. , J. C. Cote and D. Coderre . 1996 . Evaluation of coccinellid Adalia bipunctata and the invasive species Har- the effects of two Beauveria bassiana (Balsamo) Vuillemin monia axyridis (Coleoptera: Coccinellidae) . Eur. J. Entomol. strains on the development of Coleomegilla maculata lengi 105 , 437 – 443 . Timberlake (Col, Coccinellidae). J. Appl. Entomol. 120 : Warren , L. O. and M. Tadi c´ . 1967 . Biological observations in 159 – 163 . Coleomegilla maculata and its role as a predator of the fall Tourniaire , R. , A. Ferran , L. Giuge , C. Piotte and J. Gambier . webworm . J. Econ. Entomol. 60 : 1492 – 1496 . 2000 . A natural fl ightless mutation in the ladybird, Harmo- Webberley , K. M. , M. C. Tinsley , J. J. Sloggett , M. E. N. Majerus nia axyridis . Entomol. Exp. Appl. 96 : 33 – 38 . and G. D. D. Hurst . 2006 . Spatial variation in the incidence Transfaglia , A. and G. Viggiani . 1972 . Dati biologici sullo of a sexually transmitted parasite of the ladybird beetle Scymnus includens Kirsch (Coleoptera: Coccinellidae). Boll. Adalia bipunctata (Coleoptera: Coccinellidae). Eur. J. Entomol. Lab. Entomol. Agr. ‘ Philippo Silvestri’ 30 : 9 – 18 . 103 : 793 – 797 . Triltsch , H. 1996 . On the parasitization of the ladybird Coc- Williams , J. L. 1945 . The anatomy of the internal genitalia of cinella septempunctata L (Col, Coccinellidae) . J. Appl. Entomol. some Coleoptera. Proc. Entomol. Soc. Washington 47 : 120 : 375 – 378 . 73 – 91 . Trudgill , D. L. 1995 . Why do tropical poikilothermic organ- Witsack , W. 1971 . Neufunde und zur Verbreitung von Syn- isms tend to have higher threshold temperature for develop- harmonia lyncea (Ol.), einem sehn seltenen Marienk ä fer ment than temprate ones? Funct. Ecol. 9 : 136 – 137 . (Coccinellidae, Coleoptera) . Naturk. Jber. Mus. Heineanum Trudgill , D. L. , A. Hon eˇ k , D. Li and N. M. VanStraalen . 2005 . (Halberstadt) V/VI : 53 – 57 . Thermal time: concepts and utility. Ann. Appl. Biol. 146 : Wright , E. J. and J. E. Laing . 1978 . The effects on temperature 1 – 14 . on development, adult longevity and fecundity of Coleome- Ueno , H. 1994 . Itraspecifi c variation of P2 value in a coccinel- gilla maculata lengi and its parasite, Perilitus coccinellae . Proc. lid beetle, Harmonia axyridis . J. Ethol. 12 : 169 – 174 . Entomol. Soc. Ontario 109 : 33 – 47 . Ueno , H. 1996 . Estimate of multiple insemination in a natural Xia , J. Y. , W . Van der Werf and R. Rabbinge . 1999 . Tempera- population of Harmonia axyridis . Appl. Entomol. Zool. 31 : ture and prey density on bionomics of Coccinella septem- 621 – 623 . punctata (Coleoptera: Coccinellidae) feeding on Aphis Ueno , H. 2003 . Genetic variation in larval period and pupal gossypii (Homoptera: Aphididae) on cotton . Environ. mass in an aphidophagous ladybird beetle (Harmonia Entomol. 28 : 307 – 314 . axyridis ) reared in different environments . Entomol. Exp. Yakhontov , V. V. 1958 . Theoretical base for development of Appl. 106 : 211 – 218 . new method of biological control against pests. Material of Ungerov á , D. , P. Kalushkov and O. Nedv eˇ d . 2010 . Suitability 1st conference on pathology of insects and biological control, of diverse prey species for development of Harmonia Prague , 455 – 479 . (In Russian.) Life history and development 109
Yao , S. L. , Z. Huang , S. X. Ren , N. Mandour and S. Ali . 2010 . Zhu , S. R. , J. W. Su , X. H. Liu et al. 2006 . Development and Effects of temperature on development, survival, longevity, reproduction of Propylaea japonica (Coleoptera: Coccinelli- and fecundity of Serangium japonicum (Coleoptera: Coc- dae) raised on Aphis gossypii (Homoptera: Aphididae) fed cinellidae), a predator of Bemisia tabaci Gennadius (Homop- transgenic cotton. Zool. Stud. 45 : 98 – 103 . tera: Aleyrodidae). Biocontrol Sci. Tech. 21 : 23 – 34 . Yinon , U. 1969 . Food consumption of armored scale lady - beetle, Chilocorus bipustulatus (Coleoptera, Coccinellidae). Entomol. Exp. Appl. 12 : 139 – 146 .